Plasmodium knowlesi invasion following spread by infected mosquitoes, macaques and humans | Parasitology | Cambridge Core (original) (raw)

Summary

Plasmodium knowlesi is increasingly recognized as a major cause of malaria in Southeast Asia. Anopheles leucosphyrous group mosquitoes transmit the parasite and natural hosts include long-tailed and pig-tailed macaques. Despite early laboratory experiments demonstrating successful passage of infection between humans, the true role that humans play in P. knowlesi epidemiology remains unclear. The threat posed by its introduction into immunologically naïve populations is unknown despite being a public health priority for this region. A two-host species mathematical model was constructed to analyse this threat. Global sensitivity analysis using Monte Carlo methods highlighted the biological processes of greatest influence to transmission. These included parameters known to be influential in classic mosquito-borne disease models (e.g. vector longevity); however, interesting ecological components that are specific to this system were also highlighted: while local vectors likely have intrinsic preferences for certain host species, how plastic these preferences are, and how this is shaped by local conditions, are key determinants of parasite transmission potential. Invasion analysis demonstrates that this behavioural plasticity can qualitatively impact the probability of an epidemic sparked by imported infection. Identifying key vector sub/species and studying their biting behaviours constitute important next steps before models can better assist in strategizing disease control.

References

Abdullahi, M. B., Hasan, Y. A. and Abdullah, F. A. (2013). Optimal control of Plasmodium knowlesi malaria in human and macaques. British Journal of Mathematics & Computer Science 4, 271–287.Google Scholar

Abrams, P. A., Matsuda, H. and Harada, Y. (1993). Evolutionarily unstable fitness maxima and stable fitness minima of continuous traits. Evolutionary Ecology 7, 465–487.Google Scholar

Ahmed, A. M., Pinheiro, M. M., Divis, P. C., Siner, A., Zainudin, R., Wong, I. T., Lu, C. W., Singh-Khaira, S. K., Millar, S. B., Lynch, S., Willmann, M., Singh, B., Krishna, S. and Cox-Singh, J. (2014). Disease progression in Plasmodium knowlesi malaria is linked to variation in invasion gene family members. PLoS Neglected Tropical Diseases 8, e3086.Google Scholar

Anonymous (2010). Basic Population Characteristics by Administrative Districts. Malaysian Department of Statistics, Federal Government Administrative Centre, Putrajaya, Malaysia.Google Scholar

Bartlett, M. S. (1956). Deterministic and stochastic models for recurrent epidemics. In Third Berkeley Symposium on Mathematical Statistics and Probability, vol. 4 (ed. Neyman, J.), pp. 81–109. University of California Press, Berkeley.Google Scholar

Besansky, N. J., Hill, C. A. and Costantini, C. (2004). No accounting for taste: host preference in malaria vectors. Trends in Parasitology 20, 249–251.CrossRefGoogle ScholarPubMed

Bonnet, S., Gouagna, L. C., Paul, R. E., Safeukui, I., Meunier, J. Y. and Boudin, C. (2003). Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 53–59.CrossRefGoogle ScholarPubMed

Coatney, G. R., Collins, W. E., Warren, M. and Contacos, P. G. (2003). The Primate Malarias. Division of Parasitic Diseases, CDC, Atlanta, US.Google Scholar

Collins, W. E. (2012). Plasmodium knowlesi: a malaria parasite of monkeys and humans. Annual Review in Entomology 57, 107–121.Google Scholar

Cook, P. E. and Sinkins, S. P. (2010). Transcriptional profiling of Anopheles gambiae mosquitoes for adult age estimation. Insect Molecular Biology 19, 745–751.Google Scholar

Cotter, C., Gosling, R., Smith Gueye, C., Phillips, A. A., Feachem, R. G. A., Moyes, C. and Hay, S. I. (2011). Atlas of Asia Pacific Malaria Elimination Network (APMEN). University of California, San Francisco Global Health Group.Google Scholar

Cox-Singh, J., Davis, T. M. E., Lee, K.-S., Shamsul, S. S. G., Matusop, A., Ratnam, S., Rahman, H. A., Conway, D. J. and Singh, B. (2008). Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clinical Infectious Diseases 46, 165–171.Google Scholar

Diekmann, O. and Heesterbeek, J. A. P. (2000). Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis and Interpretation. Wiley, Chichester, UK.Google Scholar

Diekmann, O., Heesterbeek, J. a. P. and Roberts, M. G. (2010). The construction of next-generation matrices for compartmental epidemic models. Journal of the Royal Society Interface 7, 873–885.Google Scholar

Divis, P. C. S., Singh, B., Anderios, F., Hisam, S., Matusop, A., Kocken, C. H., Assefa, S. A., Duffy, C. W. and Conway, D. J. (2015). Admixture in humans of two divergent Plasmodium knowlesi populations associated with different macaque host species. PLoS Pathogens 11, e1004888.Google Scholar

Fornace, K. M., Nuin, N. A., Betson, M., Grigg, M. J., William, T., Anstey, N. M., Yeo, T. W., Cox, J., Ying, L. T. and Drakeley, C. J. (2015). Asymptomatic and submicroscopic carriage of Plasmodium knowlesi malaria in household and community members of clinical cases in Sabah, Malaysia. Journal of Infectious Diseases 213, 784–787.Google Scholar

Franks, S., Koram, K. A., Wagner, G. E., Tetteh, K., Mcguinness, D., Wheeler, J. G., Nkrumah, F., Ranford-Cartwright, L. and Riley, E. M. (2001). Frequent and persistent, asymptomatic Plasmodium falciparum infections in African infants, characterized by multilocus genotyping. Journal of Infectious Diseases 183, 796–804.CrossRefGoogle ScholarPubMed

Garret-Jones, C. (1964). The human blood index of malaria vectors in relation to epidemiological assessment. Bulletin of the World Health Organization 30, 241–261.Google Scholar

Gillies, M. T. (1967). Experiments on host selection in the Anopheles gambiae complex. Annals of Tropical Medicine and Parasitology 61, 68–75.Google Scholar

Imai, N., White, M. T., Ghani, A. C. and Drakeley, C. J. (2014). Transmission and control of Plasmodium knowlesi: a mathematical modelling study. PLoS Neglected Tropical Diseases 8, e2978.Google Scholar

Lee, K.-S., Divis, P. C. S., Zakaria, S. K., Matusop, A., Julin, R. A., Conway, D. J., Cox-Singh, J. and Singh, B. (2011). Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathogens 7, e1002015.Google Scholar

Liu, W., Li, Y., Learn, G. H., Rudicell, R. S., Robertson, J. D., Keele, B. F., Ndjango, J.-B. N., Sanz, C. M., Morgan, D. B., Locatelli, S., Gonder, M. K., Kranzusch, P. J., Walsh, P. D., Delaporte, E., Mpoudi-Ngole, E., Georgiev, A. V., Muller, M. N., Shaw, G. M., Peeters, M., Sharp, P. M., Rayner, J. C. and Hahn, B. H. (2010). Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425. http://www.nature.com/nature/journal/v467/n7314/abs/nature09442.html#supplementary-information.Google Scholar

Liu, W., Li, Y., Shaw, K. S., Learn, G. H., Plenderleith, L. J., Malenke, J. A., Sundararaman, S. A., Ramirez, M. A., Crystal, P. A., Smith, A. G., Bibollet-Ruche, F., Ayouba, A., Locatelli, S., Esteban, A., Mouacha, F., Guichet, E., Butel, C., Ahuka-Mundeke, S., Inogwabini, B.-I., Ndjango, J.-B. N., Speede, S., Sanz, C. M., Morgan, D. B., Gonder, M. K., Kranzusch, P. J., Walsh, P. D., Georgiev, A. V., Muller, M. N., Piel, A. K., Stewart, F. A. et al. (2014). African origin of the malaria parasite Plasmodium vivax . Nature Communications 5, 3346. doi: 10.1038/ncomms4346.Google ScholarPubMed

Lloyd, A. L., Zhang, J. and Root, A. M. (2007). Stochasticity and heterogeneity in host–vector models. Journal of the Royal Society Interface 4, 851–863.CrossRefGoogle ScholarPubMed

Macdonald, G. (1956). Epidemiological basis of malaria control. Bulletin of the World Health Organization 15, 613–626.Google Scholar

Okell, L. C., Bousema, T., Griffin, J. T., Ouedraogo, A. L., Ghani, A. C. and Drakeley, C. (2012). Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nature Communications 3, 1237.CrossRefGoogle ScholarPubMed

Pinheiro, M. M., Ahmed, M. A., Millar, S. B., Sanderson, T., Otto, T. D., Lu, W. C., Krishna, S., Rayner, J. C. and Cox-Singh, J. (2015). Plasmodium knowlesi genome sequences from clinical isolates reveal extensive genomic dimorphism. PLoS ONE 10, e0121303.Google Scholar

Reiner, R. C., Perkins, T. A., Barker, C. M., Niu, T., Chaves, L. F., Ellis, A. M., George, D. B., Le Menach, A., Pulliam, J. R. C., Bisanzio, D., Buckee, C., Chiyaka, C., Cummings, D. a. T., Garcia, A. J., Gatton, M. L., Gething, P. W., Hartley, D. M., Johnston, G., Klein, E. Y., Michael, E., Lindsay, S. W., Lloyd, A. L., Pigott, D. M., Reisen, W. K., Ruktanonchai, N., Singh, B. K., Tatem, A. J., Kitron, U., Hay, S. I., Scott, T. W. et al. (2013). A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970–2010. Journal of the Royal Society Interface 10, 20120921. doi: 10.1098/rsif.2012.0921.CrossRefGoogle ScholarPubMed

Rickman, L., Jones, T. R., Long, G. W., Paparello, S., Schneider, I., Paul, C. F., Beaudoin, R. L. and Hoffman, S. L. (1990). _Plasmodium falciparum_-infected Anopheles stephensi inconsistently transmit malaria to humans. American Journal of Tropical Medicine and Hygiene 43, 441–445.Google Scholar

Sallum, M. a. M., Peyton, E. L., Harrison, B. A. and Wilkerson, R. C. (2005). Revision of the Leucosphyrus group of Anopheles (Cellia) (Diptera, Culicidae). Revista Brasileira de Entomologia 49 (Supl. 1), 1–152. doi: 10.1590/s0085-56262005000500001.CrossRefGoogle Scholar

Singh, B. and Daneshvar, C. (2013). Human infections and detection of Plasmodium knowlesi . Clinical Microbiology Reviews 26, 165–184.Google Scholar

Singh, B., Sung, L. K., Matusop, A., Radhakrishnan, A., Shamsul, S. S. G., Cox-Singh, J., Thomas, A. and Conway, D. J. (2004). A large focus of naturally acquired Plasmodium knowlesi infections in human beings. The Lancet 363, 1017–1024.CrossRefGoogle ScholarPubMed

Smith, D. L., Battle, K. E., Hay, S. I., Barker, C. M., Scott, T. W. and Mckenzie, F. E. (2012). Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathogens 8, e1002588.Google Scholar

Takken, W. and Verhulst, N. O. (2013). Host preferences of blood-feeding mosquitoes. Annual Review in Entomology 58, 433–453.Google Scholar

Tan, C. H., Vythilingam, I., Matusop, A., Chan, S. T. and Singh, B. (2008). Bionomics of Anopheles latens in Kapit, Sarawak, Malaysian Borneo in relation to the transmission of zoonotic simian malaria parasite Plasmodium knowlesi . Malaria Journal 7, 1–8.Google Scholar

Vythilingam, I., Tan, C. H., Asmad, M., Chan, S. T., Lee, K. S. and Singh, B. (2006). Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1087–1088.Google Scholar

White, M. T., Griffin, J. T., Akpogheneta, O., Conway, D. J., Koram, K. A., Riley, E. M. and Ghani, A. C. (2014). Dynamics of the antibody response to Plasmodium falciparum infection in African children. Journal of Infectious Diseases 210, 1115–1122.Google Scholar

Who (2014). World Malaria Report 2014. World Health Organization, Geneva, Switzerland.Google Scholar

William, T., Rahman, H. A., Jelip, J., Ibrahim, M. Y., Menon, J., Grigg, M. J., Yeo, T. W., Anstey, N. M. and Barber, B. E. (2013). Increasing incidence of Plasmodium knowlesi malaria following control of P. falciparum and P. vivax malaria in Sabah, Malaysia. PLoS Neglected Tropical Diseases 7, e2026.Google Scholar

Wong, M. L., Chua, T. H., Leong, C. S., Khaw, L. T., Fornace, K., Wan-Sulaiman, W.-Y., William, T., Drakeley, C., Ferguson, H. M. and Vythilingam, I. (2015). Seasonal and spatial dynamics of the primary vector of Plasmodium knowlesi within a major transmission focus in Sabah, Malaysia. PLoS Neglected Tropical Diseases 9, e0004135.Google Scholar

Yakob, L. (2016 a). Endectocide-treated cattle for malaria control: a coupled entomological-epidemiological model. Parasite Epidemiology and Control 1, 2–9.CrossRefGoogle Scholar

Yakob, L. (2016 b). How do biting disease vectors behaviourally respond to host availability? Parasites & Vectors 9, 468.Google Scholar

Yakob, L., Bonsall, M. B. and Yan, G. (2010). Modelling knowlesi malaria transmission in humans: vector preference and host competence. Malaria Journal 9, 329.Google Scholar

Yanuar, A., Chivers, D. J., Sugardjito, J., Martyr, D. J. and Holden, J. T. (2009). The population distribution of pig-tailed macaque (Macaca nemestrina) and long-tailed macaque (Macaca fascicularis) in West Central Sumatra, Indonesia. Asian Primates Journal 1, 2–11.Google Scholar