The impact of heterogeneous transmission on the establishment and spread of antimalarial drug resistance

Journal of Theoretical Biology

Volumn 340, Issue , 2014, Pages 177-185

  Klein, Eili Y ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Center for Disease Dynamics Economics and Policy   (United States)

Author keywords

Agent based models; Drug resistance; Epidemiology; Malaria; Plasmodium falciparum

Indexed keywords

ANTIMALARIAL AGENT; ARTEMISININ;

ANTIMALARIAL AGENT; DISEASE PREVALENCE; DRUG RESISTANCE; EPIDEMIOLOGY; MALARIA; MODELING; STOCHASTICITY;

ANTIMALARIAL DRUG RESISTANCE; ARTICLE; CONCEPTUAL FRAMEWORK; DYNAMICS; HOST PARASITE INTERACTION; MALARIA; MOLECULAR DYNAMICS; PARASITE TRANSMISSION; POPULATION RESEARCH; PRIORITY JOURNAL; PROBABILITY; ROSS MACDONALD TYPE MODEL; STOCHASTIC MODEL;

SOUTHEAST ASIA;

AGENT-BASED MODELS; DRUG RESISTANCE; EPIDEMIOLOGY; MALARIA; PLASMODIUM FALCIPARUM;

ANIMALS; ANTIMALARIALS; ARTEMISININS; COMPUTER SIMULATION; CULICIDAE; DRUG RESISTANCE; HUMANS; MALARIA; MODELS, STATISTICAL; PLASMODIUM FALCIPARUM; POISSON DISTRIBUTION; STOCHASTIC PROCESSES; TIME FACTORS;

EID: 84885110475     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2013.09.022     Document Type: Article

References (67)

1. Allen G.E., Dytham C. An efficient method for stochastic simulation of biological populations in continuous time. Biosystems 2009, 98:37-42.
2. Artzy-Randrup Y., Alonso D., Pascual M. Transmission intensity and drug resistance in malaria population dynamics: implications for climate change. PLoS ONE 2010, 5:e13588.
3. Babiker H.A., Hastings I.M., Swedberg G. Impaired fitness of drug-resistant malaria parasites: evidence and implication on drug-deployment policies. Expert Review of Anti-infective Therapy 2009, 7:581-593.
4. Bailey N.T.J. The Biomathematics of Malaria 1982, C. Griffin & Co., London.
5. Barnes K.I., White N.J. Population biology and antimalarial resistance: the transmission of antimalarial drug resistance in Plasmodium falciparum. Acta Tropica 2005, 94:230-240.
6. Beier J.C., Vanderberg J.P. Sporogonic development in the mosquito. Malaria: Parasite Biology, Pathogenesis, and Protection 1998, ASM Press, Washington, D.C. I.W. Sherman (Ed.).
7. Bendixen M., Msangeni H.A., Pedersen B.V., Shayo D., Bedker R. Diversity of Plasmodium falciparum populations and complexity of infections in relation to transmission intensity and host age: a study from the Usambara Mountains, Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 2001, 95:143-148.
8. Chiyaka C., Garira W., Dube S. Effects of treatment and drug resistance on the transmission dynamics of malaria in endemic areas. Theoretical Population Biology 2009, 75:14-29.
9. Dietz K., Molineaux L., Thomas A. A malaria model tested in the African savannah. Bulletin of the World Health Organization 1974, 50:347-357.
10. Dondorp A.M., Yeung S., White L., Nguon C., Day N.P.J., Socheat D., von Seidlein L. Artemisinin resistance: current status and scenarios for containment. Nature Reviews Microbiology 2010, 8:272-280.
11. Dye C., Williams B. Multigenic drug resistance among inbred malaria parasites. Proceedings of the Royal Society of London. Series B 1997, 264:61-67.
12. Eyles D.E., Young M.D. The duration of untreated or inadequately treated Plasmodium falciparum infections in the human host. Journal of the National Malaria Society 1951, 10:327-336.
13. Felger I., Beck H.-P. Fitness costs of resistance to antimalarial drugs. Trends in Parasitology 2008, 24:331-333.
14. Fine P. Superinfection-A problem in formulating a problem. Bureau of Hygiene and Tropical Diseases 1975, 72:475-488.
15. Gatton M.L., Hogarth W., Saul A. Time of treatment influences the appearance of drug-resistant parasites in Plasmodium falciparum infections. Parasitology 2003, 123:537-546.
16. Gibson M.A., Bruck J. Efficient exact stochastic simulation of chemical systems with many species and many channels. The Journal of Physical Chemistry A 2000, 104:1876-1889.
17. Gillespie D.T. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. Journal of Computational Physics 1976, 22:403-434.
18. Gillespie D.T. Exact stochastic simulation of coupled chemical reactions. The Journal of Physical Chemistry 1977, 81:2340-2361.
19. Gillespie D.T. Approximate accelerated stochastic simulation of chemically reacting systems. Journal of Chemical Physics 2001, 115:1716-1733.
20. Hastings I.M. A model for the origins and spread of drug-resistant malaria. Parasitology 1997, 115:133-141.
21. Hastings I.M. Complex dynamics and stability of resistance to antimalarial drugs. Parasitology 2006, 132:615-624.
22. Hastings I.M., D'Alessandro U. Modelling a predictable disaster: the rise and spread of drug-resistant malaria. Parasitology Today 2000, 16:340-347.
23. Hastings I.M., Watkins W.M. Tolerance is the key to understanding antimalarial drug resistance. Trends in Parasitology 2006, 22:71-77.
24. Hethcote H.W., Yorke J.A. Gonorrhea Transmission Dynamics and Control 1984, Springer-Verlag, New York.
25. Jiang H., Patel J.J., Yi M., Mu J., Ding J., Stephens R., Cooper R.A., Ferdig M.T., Su X.-z. Genome-wide compensatory changes accompany drug-selected mutations in the Plasmodium falciparum crt gene. PLoS ONE 2008, 3:e2484.
26. Killeen G.F., McKenzie F.E., Foy B.D., Schieffelin C., Billingsley P.F., Beier J.C. A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. American Journal of Tropical Medicine and Hygiene 2000, 62:535-544.
27. Klein E. Antimalarial drug resistance: a review of the biology and strategies to delay emergence and spread. International Journal of Antimicrobial Agents 2013, 41:311-317.
28. Klein E.Y., Smith D.L., Boni M.F., Laxminarayan R. Clinically immune hosts as a refuge for drug-sensitive malaria parasites. Malaria Journal 2008, 7:67.
29. Klein E.Y., Smith D.L., Laxminarayan R., Levin S. Superinfection and the evolution of resistance to antimalarial drugs. Proc. R Soc. Biol. Sci. Ser. B 2012.
30. Knols B.G.J., de Jong R., Takken W. Differential attractiveness of isolated humans to mosquitoes in Tanzania. Proceedings of the Royal Society of London. Series B 1995, 89:604-606.
31. Lindsay S., Adiamah J.H., Miller J.E., Pleas R.J., Amstrong J.R.M. Variation in attractiveness of human subjects to malaria mosquitoes (Diptera: Culicidae) in the Gambia. Journal of Medical Entomology 1993, 30:368-373.
32. Macdonald G. The analysis of infection rates in diseases in which superinfection occurs. Tropical Diseases Bulletin 1950, 47:907-915.
33. Macdonald G. The Epidemiology and Control of Malaria 1957, Oxford University Press, London, United Kingdom.
34. Mer G., Mirnbaum D., Aioub A. The attraction of mosquitoes by human beings. Parasitology 1947, 38:1-9.
35. Nair S., Williams J.T., Brockman A., Paiphun L., Mayxay M., Newton P.N., Guthmann J.P., Smithuis F.M., Hien T.T., White N.J. A selective sweep driven by pyrimethamine treatment in southeast Asian malaria parasites. Molecular Biology and Evolution 2003, 20:1526-1536.
36. Paul R.E., Packer M.J., Walmsley M., Lagog M., Ranford-Cartwright L.C., Paru R., Day K.P. Mating patterns in malaria parasite populations of Papua New Guinea. Science 1995, 269:1709-1711.
37. Payne D. Spread of chloroquine resistance in Plasmodium falciparum. Parasitology Today 1987, 3:241-246.
38. Plowe C.V., Kublin J.G., Doumbo O.K. P. falciparum dihydrofolate reductase and dihydropteroate synthase mutations: epidemiology and role in clinical resistance to antifolates. Drug Resistance Updates 1998, 1:389-396.
39. Pongtavornpinyo W., Yeung S., Hastings I., Dondorp A., Day N., White N. Spread of anti-malarial drug resistance: mathematical model with implications for ACT drug policies. Malaria Journal 2008, 7:229.
40. Port G.R., Boreham P.F.L., Bryan J.H. The relationship of host size to feeding by mosquitoes of the Anopheles gambiae Giles complex (Diptera: Culicidae). Bulletin of Entomological Research 1980, 70:133-144.
41. Pringle G. A count of the sporozoites in an oöcyst of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 1965, 59:289-290.
42. 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., Smith D.L. A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970-2010. Journal of the Royal Society Interface 2013, 10.
43. Roper C., Pearce R., Bredenkamp B., Gumede J., Drakeley C., Mosha F., Chandramohan D., Sharp B. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet 2003, 361:1174-1181.
44. Rosenberg R., Rungsiwongse J. The number of sporozoites produced by individual malaria oocysts. American Journal of Tropical Medicine and Hygiene 1991, 45:574-577.
45. Sama W., Owusu-Agyei S., Felger I., Dietz K., Smith T. Age and seasonal variation in the transition rates and detectability of Plasmodium falciparum malaria. Parasitology 2006, 132:13-21.
46. Saul A., Graves P., Kay B. A cyclical feeding model for pathogen transmission and its application to determine vectorial capacity from vector infection rates. Journal of Applied Ecology 1990, 123-133.
47. Sinden R.E., Billingsley P.F. Plasmodium invasion of mosquito cells: hawk or dove?. Trends in Parasitology 2001, 17:209-211.
48. Smith D.L., McKenzie F.E. Statics and dynamics of malaria infection in Anopheles mosquitoes. Malaria Journal 2004, 3:13.
49. Smith D.L., Dushoff J., McKenzie F.E. The risk of a mosquito-borne infection in a heterogeneous environment. PLoS Medicine 2004, 2:e368.
50. Smith D.L., Dushoff J., Snow R.W., Hay S.I. The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature 2005, 438:492-495.
51. Smith D.L., Klein E.Y., McKenzie F.E., Laxminarayan R. Prospective strategies to delay the evolution of anti-malarial drug resistance: weighing the uncertainty. Malaria Journal 2010, 9:217.
52. Smith D.L., Drakeley C.J., Chiyaka C., Hay S.I. A quantitative analysis of transmission efficiency versus intensity for malaria. Nature Communications 2010, 1:108.
53. Smith D.L., Battle K.E., Hay S.I., Barker C.M., Scott T.W., McKenzie F.E. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathogens 2012, 8:e1002588.
54. Snow R., Trape J., Marsh K. The past, present and future of childhood malaria mortality in Africa. Trends in Parasitology 2001, 17:593-597.
55. Stoddard S.T., Morrison A.C., Vazquez-Prokopec G.M., Soldan V.P., Kochel T.J., Kitron U., Elder J.P., Scott T.W. The role of human movement in the transmission of vector-borne pathogens. PLoS Neglected Tropical Diseases 2009, 3:e481.
56. Talisuna A.O., Langi P., Mutabingwa T.K., Van Marck E., Speybroeck N., Egwang T.G., Watkins W.W., Hastings I.M., D'Alessandro U. Intensity of transmission and spread of gene mutations linked to chloroquine and sulphadoxine-pyrimethamine resistance in falciparum malaria. International Journal for Parasitology 2003, 33:1051-1058.
57. Taylor L.H., Read A. Why so Few transmission stages? reproductive restraint by malaria parasites. Parasitology Today 1997, 13:135-140.
58. Trape J.-F., Pison G., Preziosi M.-P., Enel C., du LoÛ A.D., Delaunay V., Samb B., Lagarde E., Molez J.-F., Simondon F. Impact of chloroquine resistance on malaria mortality. Comptes Rendus de l'Académie des Sciences-Series III-Sciences de la Vie 1998, 321:689-697.
59. Walton G. On the control of malaria in Freetown, Sierra Leone: 1. Plasmodium falciparum and Anopheles gambiae in relation to malaria occurring in infants. Annals of Tropical Medicine and Parasitology 1947, 41:380-407.
60. Wargo A.R., Huijben S., de Roode J.C., Shepherd J., Read A.F. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:19914-19919.
61. White N. Delaying antimalarial drug resistance with combination chemotherapy. Parassitologia 1999, 41:301-308.
62. White N. Antimalarial drug resistance and combination chemotherapy. Journal Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 1999, 354:739-749.
63. White N.J. Preventing antimalarial drug resistance through combinations. Drug Resistance Updates 1998, 1:3-9.
64. White N.J. Antimalarial drug resistance. Journal of Clinical Investigation 2004, 113:1084-1092.
65. White N.J., Pongtavornpinyo W. The de novo selection of drug-resistant malaria parasites. Proceedings of the Royal Society Series B 2003, 270:545-554.
66. Wongsrichanalai C., Pickard A.L., Wernsdorfer W.H., Meshnick S.R. Epidemiology of drug-resistant malaria. The Lancet Infectious Diseases 2002, 2:209-218.
67. 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. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:338-342.