Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T00:45:01.509Z Has data issue: false hasContentIssue false
  • English
  • Français

Of mice and men: asymmetric interactions between Bordetella pathogen species

Published online by Cambridge University Press:  11 February 2008

O. RESTIF ,
D. N. WOLFE ,
E. M. GOEBEL ,
O. N. BJORNSTAD  and
E. T. HARVILL
O. RESTIF*
Affiliation:
Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge, CB3 OES, UK
D. N. WOLFE
Affiliation:
Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, 115 Henning Building, University Park, PA 16802, USA
E. M. GOEBEL
Affiliation:
Huck Institute of Life Sciences, The Pennsylvania State University, 519 Wartik Lab, University Park, PA 16802, USA
O. N. BJORNSTAD
Affiliation:
Departments of Entomology and Biology, The Pennsylvania State University, 501 Agricultural Sciences and Industry Building, University Park, PA 16802, USA Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
E. T. HARVILL
Affiliation:
Department of Veterinary and Biomedical Sciences, The Pennsylvania State University, 115 Henning Building, University Park, PA 16802, USA
*
*Corresponding author: Cambridge Infectious Diseases Consortium, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES, UK. Tel: +44 (0)1223 337685. Fax: +44 (0)1223 764667. E-mail: or226@cam.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

In a recent experiment, we found that mice previously infected with Bordetella pertussis were not protected against a later infection with Bordetella parapertussis, while primary infection with B. parapertussis conferred cross-protection. This challenges the common assumption made in most mathematical models for pathogenic strain dynamics that cross-immunity between strains is symmetric. Here we investigate the potential consequences of this pattern on the circulation of the two pathogens in human populations. To match the empirical dominance of B. pertussis, we made the additional assumption that B. parapertussis pays a cost in terms of reduced fitness. We begin by exploring the range of parameter values that allow the coexistence of the two pathogens, with or without vaccination. We then track the dynamics of the system following the introduction of anti-pertussis vaccination. Our results suggest that (1) in order for B. pertussis to be more prevalent than B. parapertussis, the former must have a strong competitive advantage, possibly in the form of higher infectivity, and (2) because of asymmetric cross-immunity, the introduction of anti-pertussis vaccination should have little effect on the absolute prevalence of B. parapertussis. We discuss the evidence supporting these predictions, and the potential relevance of this model for other pathogens.

Keywords

whooping coughmathematical modelstrain dynamicsvaccine
Type
Research Article
Information
Parasitology , Volume 135 , Special Issue 13: Mathematical modelling of parasitic infections: from data and parameter estimation to evolutionary implications , November 2008 , pp. 1517 - 1529
Copyright
Copyright © 2008 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. and May, R. M. (1982). Directly transmitted infectious diseases: control by vaccination. Science 215, 1053–1061.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans, Oxford University Press, Oxford.CrossRefGoogle Scholar
Bergfors, E., Trollfors, B., Taranger, J., Lagergard, T., Sundh, V. and Zackrisson, G. (1999). Parapertussis and pertussis: differences and similarities in incidence, clinical course, and antibody responses. International Journal of Infectious Diseases 3, 140–146.CrossRefGoogle ScholarPubMed
Broutin, H., Rohani, P., Guégan, J.-F., Grenfell, B. T. and Simondon, F. (2004). Loss of immunity to pertussis in a rural community in Senegal. Vaccine 22, 594–596.CrossRefGoogle Scholar
Centers for Disease Control and Prevention (2007). Nationally notifiable infectious diseases, United States 2007, revised. Centers for Disease Control and Prevention, Atlanta.Google Scholar
Cimolai, N. and Trombley, C. (2001). Molecular diagnostics confirm the paucity of parapertussis activity. European Journal of Pediatrics 160, 518–525.CrossRefGoogle ScholarPubMed
Diavatopoulos, D. A., Cummings, C. A., Schouls, L. M., Brinig, M. M., Relman, D. A. and Mooi, F. R. (2005). Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. Public Library of Science Pathogens 1, 45–55.Google ScholarPubMed
Dragsted, D. M., Dohn, B., Madsen, J. and Jensen, J. S. (2004). Comparison of culture and PCR for detection of Bordetella pertussis and Bordetella parapertussis under routine laboratory conditions. Journal of Medical Microbiology 53, 749–754.CrossRefGoogle ScholarPubMed
Earn, D. J. D., Rohani, P., Bolker, B. and Grenfell, B. T. (2000). A simple model for complex dynamical transitions in epidemics. Science 287, 667–670.CrossRefGoogle ScholarPubMed
Elbasha, E. H. and Galvani, A. P. (2005). Vaccination against multiple HPV types. Mathematical Biosciences 197, 88–117.CrossRefGoogle ScholarPubMed
Eldering, G. and Kendrick, P. (1938). Bacillus para-pertussis: a species resembling both Bacillus pertussis and Bacillus bronchisepticus but identical with neither. Journal of Bacteriology 35, 561–572.CrossRefGoogle Scholar
Eldering, G. and Kendrick, P. (1952). Incidence of parapertussis in the Grand Rapids Area as indicated by 16 years' experience with diagnostic cultures. American Journal of Public Health and the Nation's Health 42, 27–31.CrossRefGoogle Scholar
Ferguson, N. M., Galvani, A. P. and Bush, R. M. (2003). Ecological and immunological determinants of influenza evolution. Nature 422, 428–433.CrossRefGoogle ScholarPubMed
Frank, S. A. and Barbour, A. G. (2006). Within-host dynamics of antigenic variation. Infection, Genetics and Evolution 6, 141–146.CrossRefGoogle ScholarPubMed
Frühwirth, M., Neher, C., Schmidt-Schläpfer, G. and Allerberger, F. (2002). Bordetella pertussis and Bordetella parapertussis infection in an Austrian pediatric outpatient clinic. Wiener klinische Wochenschrift 114, 377–382.Google Scholar
Gandon, S. and Day, T. (2007). The evolutionary epidemiology of vaccination. Journal of the Royal Society Interface 4, 803–817.CrossRefGoogle ScholarPubMed
Gandon, S., Mackinnon, M. J., Nee, S. and Read, A. F. (2001). Imperfect vaccines and the evolution of pathogen virulence. Nature 414, 751–756.CrossRefGoogle ScholarPubMed
Genton, B., Betuela, I., Felger, I., Al-Yaman, F., Anders, R. F., Saul, A., Rare, L., Baisor, M., Lorry, K., Brown, G. V., Pye, D., Irving, D. O., Smith, T. A., Beck, H.-P. and Alpers, M. P. (2002). A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1–2b trial in Papua New Guinea. Journal of Infectious Diseases 185, 820–827.CrossRefGoogle Scholar
Gog, J. and Grenfell, B. T. (2002). Dynamics and selection of many-strain pathogens. Proceedings of the National Academy of Sciences, USA 99, 17209–17214.CrossRefGoogle ScholarPubMed
Gog, J. and Swinton, J. (2002). A status-based approach to multiple strain dynamics. Journal of Mathematical Biology 44, 169–184.CrossRefGoogle ScholarPubMed
Gomes, M. G. M., Medley, G. F. and Nokes, D. J. (2002). On the determinants of population structure in antigenically diverse pathogens. Proceedings of the Royal Society of London, Series B 269, 227–233.CrossRefGoogle ScholarPubMed
Granström, M. and Askelöf, P. (1982). Parapertussis: an abortive pertussis infection? The Lancet 320, 1233–1290.CrossRefGoogle Scholar
Grenfell, B. T., Pybus, O. G., Gog, J. R., Wood, J. L. N., Daly, J. M., Mumford, J. A. and Holmes, E. C. (2004). Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327–332.CrossRefGoogle ScholarPubMed
Gupta, S., Ferguson, N. M. and Anderson, R. M. (1997). Vaccination and the population structure of antigenically diverse pathogens that exchange genetic material. Proceedings of the Royal Society of London, Series B 264, 1435–1443.CrossRefGoogle ScholarPubMed
He, Q., Arvilommi, H., Viljanen, M. K. and Mertsola, J. (1999). Outcomes of Bordetella infection in vaccinated children: effects of bacterial number in the nasopharynx and patient age. Clinical and Diagnostic Laboratory Immunology 6, 534–536.CrossRefGoogle ScholarPubMed
He, Q., Viljanen, M. K., Arvilommi, H., Aittanen, B. and Mertsola, J. (1998). Whooping cough caused by Bordetella pertussis and Bordetella parapertussis in an immunized population. Journal of the American Medical Association 260, 635–637.CrossRefGoogle Scholar
Kamo, M. and Sasaki, A. (2002). The effects of cross-immunity and seasonal forcing in a multi-strain epidemic model. Physica D 165, 228–241.CrossRefGoogle Scholar
Khelef, N., Danve, B., Quentin-Millet, M.-J. and Guiso, N. (1993). Bordetella pertussis and Bordetella parapertussis: two immunologically distinct species. Infection and Immunity 61, 486–490.CrossRefGoogle ScholarPubMed
Kitching, R. P., Taylor, N. M. and Thrusfield, M. V. (2007). Vaccination strategies for foot-and-mouth disease. Nature 445, E12.CrossRefGoogle ScholarPubMed
Koelle, K., Cobey, S., Grenfell, B. T. and Pascual, M. (2006). Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 314, 1898–1903.CrossRefGoogle ScholarPubMed
Lautrop, H. (1958). Observations on parapertussis in Denmark. Acta Pathologica et Microbiologica Scandinavica 43, 255–266.CrossRefGoogle ScholarPubMed
Lautrop, H. (1971). Epidemics of parapertussis – 20 years’ observations in Denmark. The Lancet 297, 1195–1198.CrossRefGoogle Scholar
Letowska, I. and Hryniewicz, W. (2004). Epidemiology and characterization of Bordetella parapertussis strains isolated between 1995 and 2002 in and around Warsaw, Poland. European Journal of Clinical Microbiology and Infectious Diseases 23, 499–501.CrossRefGoogle ScholarPubMed
Liese, J. G., Renner, C., Stojanov, S., Belohradsky, B. H. and The Munich Vaccine Study Group (2003). Clinical and epidemiological picture of B. pertussis and B. parapertussis infections after introduction of acellular pertussis vaccines. Archives of Disease in Childhood 88, 684–687.CrossRefGoogle Scholar
Lipsitch, M. (1997). Vaccination against colonizing bacteria with multiple serotypes. Proceedings of the National Academy of Sciences, USA 94, 6571–6576.CrossRefGoogle ScholarPubMed
Lipsitch, M., Dykes, J. K., Johnson, S. E., Ades, E. W., King, J., Briles, D. E. and Carlone, G. M. (2000). Competition among Streptococcus pneumoniae for intranasal colonization in a mouse model. Vaccine 18, 2895–2901.CrossRefGoogle ScholarPubMed
Mastrantonio, P., Stefanelli, P., Giuliano, M., Herrera Rojas, Y., Ciofi Degli Atti, M. L., Anemona, A. and Tozzi, A. E. (1998). Bordetella parapertussis infection in children: epidemiology, clinical symptoms, and molecular characteristics of isolates. Journal of Clinical Microbiology 36, 999–1002.CrossRefGoogle ScholarPubMed
Mattoo, S. and Cherry, J. D. (2005). Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clinical Microbiology Reviews 18, 326–382.CrossRefGoogle ScholarPubMed
Mclean, A. R. (1995). Vaccination, evolution and changes in the efficacy of vaccines: a theoretical framework. Proceedings of the Royal Society of London, Series B 261, 389–393.Google ScholarPubMed
McMichael, A., Mwau, M. and Hanke, T. (2002). HIV T cell vaccines, the importance of clades. Vaccine 20, 1918–1921.CrossRefGoogle Scholar
Musser, J. M., Hewlett, E. L., Peppler, M. S. and Selander, R. K. (1986). Genetic diversity and relationships in populations of Bordetella spp. Journal of Bacteriology 166, 230–237.CrossRefGoogle ScholarPubMed
Olin, P., Gustafsson, L., Barreto, L., Hessel, L., Mast, T. C., Van Rie, A., Bogaerts, H. and Storsaeter, J. (2003). Declining pertussis incidence in Sweden following the introduction of acellular pertussis vaccine. Vaccine 21, 2015–2021.CrossRefGoogle ScholarPubMed
Park, A. W., Wood, J. L. N., Daly, J. M., Newton, J. R., Glass, K., Henley, W., Mumford, J. A. and Grenfell, B. T. (2004). The effects of strain heterology on the epidemiology of equine influenza in a vaccinated population. Proceedings of the Royal Society of London, Series B 271, 1547–1555.CrossRefGoogle Scholar
Redhead, K., Watkins, J., Barnard, A. and Mills, K. H. (1993). Effective immunization against Bordetella pertussis respiratory infection in mice is dependent on induction of cell-mediated immunity. Infection and Immunity 61, 3190–3198.CrossRefGoogle ScholarPubMed
Restif, O. and Grenfell, B. T. (2007). Vaccination and the dynamics of immune evasion. Journal of the Royal Society Interface 4, 143–153.CrossRefGoogle ScholarPubMed
Rohani, P., Keeling, M. J. and Grenfell, B. T. (2002). The interplay between determinism and stochasticity in childhood diseases. American Naturalist 159, 469–481.CrossRefGoogle ScholarPubMed
Sato, H. and Sato, Y. (1984). Bordetella pertussis infection in mice: correlation of specific antibodies against two antigens, pertussis toxin, and filamentous hemagglutinin with mous protectivity in an intracerebral or aerosol challenge system. Infection and Immunity 46, 415–421.CrossRefGoogle ScholarPubMed
Sato, Y., Izumiya, K., Sato, H., Cowell, J. L. and Manclark, C. R. (1980). Aerosol infection of mice with Bordetella pertussis. Infection and Immunity 29, 261–266.CrossRefGoogle ScholarPubMed
Smith, D. J., Lapedes, A. S., De Jong, J. C., Bestebroer, T. M., Rimmelzwaan, G. F., Osterhaus, A. D. M. E. and Fouchier, R. A. M. (2004). Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371–376.CrossRefGoogle ScholarPubMed
Smith, T. (2002). Imperfect vaccines and imperfect models. Trends in Ecology and Evolution 17, 154–156.CrossRefGoogle Scholar
Stehr, K., Cherry, J. D., Heininger, U., Schmitt-Grohé, S., Überall, M., Laussucq, S., Eckhardt, T., Meyer, M., Engelhardt, R., Christenson, P. and Group, T. P. V. S. (1998). A comparative efficacy trial in Germany in infants who received either the Lederle/Takeda acellular pertussis component DTP (DTaP) vaccine, the Lederle whole-cell component DTP vaccine, or DT vaccine. Pediatrics 101, 1–12.CrossRefGoogle ScholarPubMed
Stibitz, S. and Yang, M.-S. (1997). Genomic fluidity of Bordetella pertussis assessed by a new method for chromosomal mapping. Journal of Bacteriology 179, 5820–5826.CrossRefGoogle ScholarPubMed
Tildesley, M. J., Savill, N. J., Shaw, D. J., Deardon, R., Brooks, S. P., Woolhouse, M. E. J., Grenfell, B. T. and Keeling, M. J. (2006). Optimal reactive vaccination strategies for a foot-and-mouth outbreak in the UK. Nature 440, 83–86.CrossRefGoogle ScholarPubMed
Watanabe, M. and Nagai, M. (2001). Reciprocal protective immunity against Bordetella pertussis and Bordetella parapertussis in a murine model of respiratory infection. Infection and Immunity 69, 6981–6986.CrossRefGoogle Scholar
Wearing, H. J. and Rohani, P. (2006). Ecological and immunological determinants of dengue epidemics. Proceedings of the National Academy of Sciences, USA 103, 11802–11807.CrossRefGoogle ScholarPubMed
White, L. J., Cox, M. J. and Medley, G. F. (1998). Cross immunity and vaccination against multiple microparasite strains. IMA Journal of Mathematics Applied in Medicine and Biology 15, 211–233.CrossRefGoogle ScholarPubMed
Willems, R. J. L., Kamerbeek, J., Geuijen, C. A. W., Top, J., Gielen, H., Gaastra, W. and Mooi, F. R. (1998). The efficacy of a whole cell pertussis vaccine and fimbriae against Bordetella pertussis and Bordetella parapertussis infections in a respiratory mouse model. Vaccine 16, 410–416.CrossRefGoogle Scholar
Wilson, J. N., Nokes, D. J. and Carman, W. F. (1999). The predicted pattern of emergence of vaccine-resistant hepatitis B: a cause for concern? Vaccine 17, 973–978.CrossRefGoogle ScholarPubMed
Wolfe, D. N., Goebel, E. M., Bjørnstad, O. N., Restif, O. and Harvill, E. T. (2007). The O antigen enables Bordetella parapertussis to avoid Bordetella pertussis-induced immunity. Infection and Immunity 75, 4972–4979.CrossRefGoogle ScholarPubMed
Wolfram, S. (2007). The Mathematica Book, 6th Edition, Wolfram Media.Google Scholar
Zhang, Y., Auranen, K. and Eichner, M. (2004). The influence of competition and vaccination on the coexistence of two pneumococcal serotypes. Epidemiology and Infection 132, 1073–1081.CrossRefGoogle ScholarPubMed