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HIV-1/parasite co-infection and the emergence of new parasite strains

Published online by Cambridge University Press:  27 March 2008

JAMES O. LLOYD-SMITH ,
MARY POSS  and
BRYAN T. GRENFELL
JAMES O. LLOYD-SMITH*
Affiliation:
Center for Infectious Disease Dynamics, Pennsylvania State University, 208 Mueller Lab, University Park PA, 16802, USA
MARY POSS
Affiliation:
Center for Infectious Disease Dynamics, Pennsylvania State University, 208 Mueller Lab, University Park PA, 16802, USA
BRYAN T. GRENFELL
Affiliation:
Center for Infectious Disease Dynamics, Pennsylvania State University, 208 Mueller Lab, University Park PA, 16802, USA Fogarty International Center, US National Institutes of Health, Bethesda MD, 20892, USA
*
*Corresponding author. Tel: +1-814-863-9545. Fax: +1-814-865-9131. E-mail: [email protected]
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Summary

HIV-1 and parasitic infections co-circulate in many populations, and in a few well-studied examples HIV-1 co-infection is known to amplify parasite transmission. There are indications that HIV-1 interacts significantly with many other parasitic infections within individual hosts, but the population-level impacts of co-infection are not well-characterized. Here we consider how alteration of host immune status due to HIV-1 infection may influence the emergence of novel parasite strains. We review clinical and epidemiological evidence from five parasitic diseases (malaria, leishmaniasis, schistosomiasis, trypanosomiasis and strongyloidiasis) with emphasis on how HIV-1 co-infection alters individual susceptibility and infectiousness for the parasites. We then introduce a simple modelling framework that allows us to project how these individual-level properties might influence population-level dynamics. We find that HIV-1 can facilitate invasion by parasite strains in many circumstances and we identify threshold values of HIV-1 prevalence that allow otherwise unsustainable parasite strains to invade successfully. Definitive evidence to test these predicted effects is largely lacking, and we conclude by discussing challenges in interpreting available data and priorities for future studies.

Keywords

HIV/AIDSemerging infectious diseasesmathematical modelpopulation heterogeneitydrug resistancezoonosisimmunosuppression
Type
Original Articles
Information
Parasitology , Volume 135 , Special Issue 7: Parasitic co-infections: challenges and solutions , June 2008 , pp. 795 - 806
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Abu-Raddad, L. J., Patnaik, P. and Kublin, J. G. (2006). Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314, 1603–1606.CrossRefGoogle ScholarPubMed
Ambroise-Thomas, P. (2001). Parasitic diseases and immunodeficiencies. Parasitology 122, S65–S71.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control, Oxford University Press, UK.CrossRefGoogle Scholar
Andre, J. B. and Day, T. (2005). The effect of disease life history on the evolutionary emergence of novel pathogens. Proceedings of the Royal Society B-Biological Sciences 272, 1949–1956.CrossRefGoogle ScholarPubMed
Antia, R., Regoes, R. R., Koella, J. C. and Bergstrom, C. T. (2003). The role of evolution in the emergence of infectious diseases. Nature 426, 658–661.CrossRefGoogle ScholarPubMed
Becker, N. and Marschner, I. (1990). The effect of heterogeneity on the spread of disease. In Stochastic Processes in Epidemic Theory, Vol. 86 (eds. Picard, P., Gabriel, J. P. and Lefevre, C.), pp. 90–103. Springer-Verlag, New York.CrossRefGoogle Scholar
Brown, M., Mawa, P. A., Kaleebu, P. and Elliott, A. M. (2006). Helminths and HIV infection: epidemiological observations on immunological hypotheses. Parasite Immunology 28, 613–623.CrossRefGoogle ScholarPubMed
Butcher, G. A. (2005). T-cell depletion and immunity to malaria in HIV-infections. Parasitology 130, 141–150.CrossRefGoogle ScholarPubMed
Chicharro, C. and Alvar, J. (2003). Lower trypanosomatids in HIV/AIDS patients. Annals of Tropical Medicine and Parasitology 97, 75–78.CrossRefGoogle ScholarPubMed
Chicharro, C., Jimenez, M. I. and Alvar, J. (2003). Iso-enzymatic variability of Leishmania infantum in Spain. Annals of Tropical Medicine and Parasitology 97, 57–64.CrossRefGoogle ScholarPubMed
Corbett, E. L., Steketee, R. W., ter Kuile, F. O., Latif, A. S., Kamali, A. and Hayes, R. J. (2002). HIV-1/AIDS and the control of other infectious diseases in Africa. Lancet 359, 2177–2187.CrossRefGoogle ScholarPubMed
Croft, S. L., Sundar, S. and Fairlamb, A. H. (2006). Drug resistance in leishmaniasis. Clinical Microbiology Reviews 19, 111–126.CrossRefGoogle ScholarPubMed
Cross, P. C., Lloyd-Smith, J. O., Johnson, P. L. F. and Getz, W. M. (2005). Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations. Ecology Letters 8, 587–595.CrossRefGoogle Scholar
Davies, S. J., Grogan, J. L., Blank, R. B., Lim, K. C., Locksley, R. M. and McKerrow, J. H. (2001). Modulation of blood fluke development in the liver by hepatic CD4(+) lymphocytes. Science 294, 1358–1361.CrossRefGoogle ScholarPubMed
Desjeux, P. and Alvar, J. (2003). Leishmania/HIV co-infections: epidemiology in Europe. Annals of Tropical Medicine and Parasitology 97, 3–15.CrossRefGoogle ScholarPubMed
Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis, and Interpretation, John Wiley & Sons, Chichester.Google Scholar
Doenhoff, M. J., Hassounah, O., Murare, H., Bain, J. and Lucas, S. (1986). The schistosome egg granuloma – immunopathology in the cause of host protection or parasite survival. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 503–514.CrossRefGoogle ScholarPubMed
French, N., Nakiyingi, J., Lugada, E., Watera, C., Whitworth, J. A. G. and Gilks, C. F. (2001). Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. AIDS 15, 899–906.CrossRefGoogle ScholarPubMed
Graham, A. L., Cattadori, I. M., Lloyd-Smith, J. O., Ferrari, M. J. and Bjornstad, O. N. (2007). Transmission consequences of coinfection: cytokines writ large Trends in Parasitology 23, 284–291.CrossRefGoogle ScholarPubMed
Gramiccia, M. (2003). The identification and variability of the parasites causing leishmaniasis in HIV-positive patients in Italy. Annals of Tropical Medicine and Parasitology 97, 65–73.CrossRefGoogle ScholarPubMed
Gupta, S., Swinton, J. and Anderson, R. M. (1994). Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of the Royal Society of London Series B-Biological Sciences 256, 231–238.Google ScholarPubMed
Harms, G. and Feldmeier, H. (2005). The impact of HIV infection on tropical diseases. Infectious Disease Clinics of North America 19, 121–135.CrossRefGoogle ScholarPubMed
Harris, T. E. (1963). The Theory of Branching Processes, Springer, Berlin.CrossRefGoogle Scholar
Kaare, M., Picozzi, K., Mlengeya, T., Fèvre, E., Mellau, L., Mtambo, M., Cleaveland, S. and Welburn, S. (2007). Sleeping sickness – A re-emerging disease in the Serengeti Travel Medicine and Infectious Disease 5, 117–124.CrossRefGoogle ScholarPubMed
Kibona, S. N., Matemba, L., Kaboya, J. S. and Lubega, G. W. (2006). Drug-resistance of Trypanosoma b. rhodesiense isolates from Tanzania. Tropical Medicine and International Health 11, 144–155.CrossRefGoogle ScholarPubMed
Korenromp, E. L., Williams, B. G., de Vlas, S. J., Gouws, E., Gilks, C. F., Ghys, P. D. and Nahlen, B. L. (2005). Malaria attributable to the HIV-1 epidemic, sub-Saharan Africa. Emerging Infectious Diseases 11, 1410–1419.CrossRefGoogle Scholar
Laguna, F. (2003). Treatment of leishmaniasis in HIV-positive patients. Annals of Tropical Medicine and Parasitology 97, 135–142.CrossRefGoogle ScholarPubMed
Legros, D., Evans, S., Maiso, F., Enyaru, J. C. K. and Mbulamberi, D. (1999). Risk factors for treatment failure after melarsoprol for Trypanosoma brucei gambiense trypanosomiasis in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 439–442.CrossRefGoogle ScholarPubMed
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.CrossRefGoogle ScholarPubMed
Mathis, A., Weber, R. and Deplazes, P. (2005). Zoonotic potential of the microsporidia. Clinical Microbiology Reviews 18, 423–445.CrossRefGoogle ScholarPubMed
Matovu, E., Seebeck, T., Enyaru, J. C. K. and Kaminsky, R. (2001). Drug resistance in Trypanosoma brucei spp., the causative agents of sleeping sickness in man and nagana in cattle. Microbes and Infection 3, 763–770.CrossRefGoogle ScholarPubMed
Mermin, J., Lule, J., Ekwaru, J. P., Downing, R., Hughes, P., Bunnell, R., Malamba, S., Ransom, R., Kaharuza, F., Coutinho, A., Kigozi, A. and Quick, R. (2005). Cotrimoxazole prophylaxis by HIV-infected persons in Uganda reduces morbidity and mortality among HIV-uninfected family members. AIDS 19, 1035–1042.CrossRefGoogle ScholarPubMed
Molina, R., Gradoni, L. and Alvar, J. (2003). HIV and the transmission of Leishmania. Annals of Tropical Medicine and Parasitology 97, 29–45.CrossRefGoogle ScholarPubMed
Pieniazek, N. J., Bornay-Llinares, F. J., Slemenda, S. B., da Silva, A. J., Moura, I. N. S., Arrowood, M. J., Ditrich, O. and Addiss, D. G. (1999). New Cryptosporidium genotypes in HIV-infected persons. Emerging Infectious Diseases 5, 444–449.CrossRefGoogle ScholarPubMed
Porco, T. C., Small, P. M. and Blower, S. M. (2001). Amplification dynamics: Predicting the effect of HIV on tuberculosis outbreaks. Journal of Acquired Immune Deficiency Syndromes 28, 437–444.CrossRefGoogle ScholarPubMed
Pratlong, F., Dereure, J., Deniau, M., Marty, P., Faraut-Gambarelli, F. and Dedet, J. P. (2003). Enzymatic polymorphism during Leishmania/HIV co-infection: a study of 381 Leishmania strains received between 1986 and 2000 at the international cryobank in Montpellier, France. Annals of Tropical Medicine and Parasitology 97, 47–56.CrossRefGoogle ScholarPubMed
Redhu, N. S., Dey, A., Balooni, V. and Singh, S. (2006). Leishmania-HIV co-infection: an emerging problem in India. AIDS 20, 1213–1214.CrossRefGoogle ScholarPubMed
Secor, W. E. (2006). Interactions between schistosomiasis and infection with HIV-1. Parasite Immunology 28, 597–603.CrossRefGoogle ScholarPubMed
Taylor, H. M. and Karlin, S. (1998). An Introduction to Stochastic Modeling, 3 edn.Academic Press, San Diego.Google Scholar
Ter Kuile, F. O., Parise, M. E., Verhoeff, F. H., Udhayakumar, V., Newman, R. D., Van Eijk, A. M., Rogerson, S. J. and Steketee, R. W. (2004). The burden of co-infection with human immunodeficiency virus type 1 and malaria in pregnant women in sub-Saharan Africa. American Journal of Tropical Medicine and Hygiene 71, 41–54.CrossRefGoogle ScholarPubMed
UNAIDS (2006). Report on the global AIDS epidemic. Joint United Nations Programme on HIV/AIDS, Geneva.Google Scholar
Van Geertruyden, J. P., Mulenga, M., Mwananyanda, L., Chalwe, V., Moerman, F., Chilengi, R., Kasongo, W., Van Overmeir, C., Dujardin, J. C., Colebunders, R., Kestens, L. and D'Alessandro, U. (2006). HIV-1 immune suppression and antimalarial treatment outcome in Zambian adults with uncomplicated malaria. Journal of Infectious Diseases 194, 917–925.CrossRefGoogle ScholarPubMed
Viney, M. E., Brown, M., Omoding, N. E., Bailey, J. W., Gardner, M. P., Roberts, E., Morgan, D., Elliott, A. M. and Whitworth, J. A. G. (2004). Why does HIV infection not lead to disseminated strongyloidiasis Journal of Infectious Diseases 190, 2175–2180.CrossRefGoogle Scholar
White, N. J. (2004). Antimalarial drug resistance. Journal of Clinical Investigation 113, 1084–1092.CrossRefGoogle ScholarPubMed
Whitworth, J. (2006). Malaria and HIV. In HIV InSite Knowledge Base, Vol. 2007 (eds. Peiperl, L., Coffey, S., Bacon, O. and Voberding, P.), URL http://hivinsite.ucsf.edu/InSite?page=k6-05-04-0. (Accessed Oct 14, 2007). UCSF Center for HIV Information, San Francisco.Google Scholar
Whitworth, J., Morgen, D., Quigley, M., Smith, A., Mayanja, S., Eotu, H., Omoding, N., Okongo, M., Malamba, S. and Ojwiya, A. (2000). Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet 356, 1051–1056.CrossRefGoogle ScholarPubMed
Williams, B. G. and Dye, C. (2003). Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science 301, 1535–1537.CrossRefGoogle ScholarPubMed
Williams, B. G., Korenromp, E. L., Gouws, E., Schmid, G. P., Auvert, B. and Dye, C. (2006). HIV infection, Antiretroviral therapy, and CD4(+) cell count distributions in African populations. Journal of Infectious Diseases 194, 1450–1458.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. (1997). Heteropeneities in the transmission of infectious agents Implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338–342.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J., Haydon, D. T. and Antia, R. (2005). Emerging pathogens: the epidemiology and evolution of species jumps. Trends in Ecology and Evolution 20, 238–244.CrossRefGoogle ScholarPubMed
Yates, A., Antia, R. and Regoes, R. R. (2006). How do pathogen evolution and host heterogeneity interact in disease emergence Proceedings of the Royal Society B-Biological Sciences 273, 3075–3083.CrossRefGoogle ScholarPubMed