Abstract
Technologies for strain differentiation and typing have made it possible to detect genetic diversity of pathogens, both within individual hosts and within communities. Coinfection of a host by more than one pathogen strain may affect the relative frequency of these strains at the population level through complex within- and between-host interactions; in infectious diseases that have a long latent period, interstrain competition during latency is likely to play an important role in disease dynamics. We show that SEIR models that include a class of latently coinfected individuals can have markedly different long-term dynamics than models without coinfection, and that coinfection can greatly facilitate the stable coexistence of strains. We demonstrate these dynamics using a model relevant to tuberculosis in which people may experience latent coinfection with both drug sensitive and drug resistant strains. Using this model, we show that the existence of a latent coinfected state allows the possibility that disease control interventions that target latency may facilitate the emergence of drug resistance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adler, F.R., Losada, J.M., 2002. Super-and coinfection: filling the range. In: Dieckmann, U. (Ed.), Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management, pp. 139–149. Cambridge University Press, Cambridge.
Almeida, A.M.F., Matsumoto, M.T., Baeza, L.C., Silva, R., Aparecida, A., Kleiner, A., Melhem, M., Giannini, M., 2007. Molecular typing and antifungal susceptibility of clinical sequential isolates of cryptococcus neoformans from Sao Paulo state, Brazil. FEMS Yeast Res. 7(1), 152–164.
Aziz, M.A., Wright, A., 2005. The world health organization/international union against tuberculosis and lung disease global project on surveillance for anti-tuberculosis drug resistance: a model for other infectious diseases. Clin. Infect. Dis. 41(Suppl 4), S258–S262.
Carrillo, F.Y.E., Sanjuán, R., Moya, A., Cuevas, J.M., 2007. The effect of co-and superinfection on the adaptive dynamics of vesicular stomatitis virus. Infect. Genet. Evol. 7(1), 69–73.
Casado, C., Pernas, M., Alvaro, T., Sandonis, V., Garcia, S., Rodriguez, C., del Romero, J., Grau, E., Ruiz, L., Lopez-Galindez, C., 2007. Coinfection and superinfection in patients with long-term, nonprogressive HIV-1 disease. J. Infect. Dis. 196(6), 895–899.
Claessen, D., de Roos, A.M., 1995. Evolution of virulence in a host-pathogen system with local pathogen transmission. Oikos 74(3), 401–413.
Cohen, T., Lipsitch, M., Walensky, R.P., Murray, M., 2006. Beneficial and perverse effects of isoniazid preventive therapy for latent tuberculosis infection in HIV–tuberculosis coinfected populations. Proc. Natl. Acad. Sci. 103(18), 7042–7047.
Davies, A.P., Billington, O.J., Bannister, B.A., Weir, W.R., McHugh, T.D., Gillespie, S.H., 2000. Comparison of fitness of two isolates of mycobacterium tuberculosis, one of which had developed multi-drug resistance during the course of treatment. J. Infect. 41(2), 184–187.
Eames, K.T.D., Keeling, M.J., 2006. Coexistence and specialization of pathogen strains on contact networks. Am. Nat. 168(2), 230–241.
Elbasha, E.H., Galvani, A.P., 2005. Vaccination against multiple HPV types. Math. Biosci. 197(1), 88–117.
Gandhi, N., Moll, A., Willem Sturm, A., Pawinski, R., Govender, T., Lalloo, U., Zeller, K., Andrews, J., Friedland, G., 2006. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368(9547), 1575–1580.
Iannelli, M., Martcheva, M., Li, X.Z., 2005. Strain replacement in an epidemic model with superinfection and perfect vaccination. Math. Biosci. 195(1), 23–46.
Levin, S., Pimentel, D., 1981. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117(3), 308–315.
Levin, S.A., 1983. Some approaches to the modeling of coevolutionary interactions. In: Coevolution, pp. 21–65. University of Chicago Press, Chicago.
Li, J., Ma, Z., Blythe, S.P., Castillo-Chavez, C., 2003. Coexistence of pathogens in sexually-transmitted disease models. J. Math. Biol. 47(6), 547–568.
Li, X., Zhang, Y., Shen, X., Shen, G., Gui, X., Sun, B., et al., 2007. Transmission of drug-resistant tuberculosis among treated patients in Shanghai, China. J. Infect. Dis. 195(6), 864–869.
Lipsitch, M., 1997. Vaccination against colonizing bacteria with multiple serotypes. Proc. Natl. Acad. Sci. 94(12), 6571–6576.
Martcheva, M., Pilyugin, S.S., Holt, R.D., 2007. Subthreshold and superthreshold coexistence of pathogen variants: the impact of host age-structure. Math. Biosci. 207(1), 58–77.
May, R.M., Nowak, M.A., 1995. Coinfection and the evolution of parasite virulence. Proc. Biol. Sci. 261(1361), 209–215.
Mosquera, J., Adler, F.R., 1998. Evolution of virulence: a unified framework for coinfection and superinfection. J. Theor. Biol. 195(3), 293–313.
Murrell, D.J., Law, R., 2003. Heteromyopia and the spatial coexistence of similar competitors. Ecol. Lett. 6(1), 48–59.
Rattan, A., Kalia, A., Ahmad, N., 1998. Multidrug-resistant mycobacterium tuberculosis: molecular perspectives. Emerg. Infect. Dis. 4(2), 195–209.
Rodrigues, P., Gomes, M.G.M., Rebelo, C., 2007. Drug resistance in tuberculosis—a reinfection model. Theor. Popul. Biol. 71(2), 196–212.
Schinazi, R.B., 1997. Predator-prey and host-parasite spatial stochastic models. Ann. Appl. Probab. 7(1), 1–9.
Shigidi, M., Hashim, R., Idris, M., Mukhtar, M., Sokrab, T., 2004. Parasite diversity in adult patients with cerebral malaria: a hospital-based, case-control study. Am. J. Trop. Med. Hyg. 71(6), 754–757.
Troyer, R.M., Collins, K.R., Abraha, A., Fraundorf, E., Moore, D.M., Krizan, R.W., Toossi, Z., Colebunders, R.L., Jensen, M.A., Mullins, J.I., et al., 2005. Changes in human immunodeficiency virus type 1 fitness and genetic diversity during disease progression. J. Virol. 79(14), 9006.
van Rie, A., Victor, T., Richardson, M., Johnson, R., van der Spuy, G., Murray, E., Beyers, N., van Pittius, N., van Helden, P., Warren, R., 2005. Reinfection and mixed infection cause changing mycobacterium tuberculosis drug-resistance patterns. Am. J. Respir. Crit. Care Med. 172(5), 636–642.
Warren, R.M., Victor, T.C., Streicher, E.M., Richardson, M., Beyers, N., van Pittius, N.C.G., van Helden, P.D., 2004. Patients with active tuberculosis often have different strains in the same sputum specimen. Am. J. Respir. Crit. Care Med. 169(5), 610.
Wodarz, D., Levy, D.N., 2007. Human immunodeficiency virus evolution towards reduced replicative fitness in vivo and the development of AIDS. Proc. R. Soc. B: Biol. Sci. 274(1624), 2481–2490.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Colijn, C., Cohen, T. & Murray, M. Latent Coinfection and the Maintenance of Strain Diversity. Bull. Math. Biol. 71, 247–263 (2009). https://doi.org/10.1007/s11538-008-9361-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11538-008-9361-y