Dissecting the determinants of malaria chronicity: Why within-host models struggle to reproduce infection dynamics

Journal of the Royal Society Interface

Volumn 12, Issue 104, 2015, Pages

  Childs, Lauren M ^a   Buckee, Caroline O ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Chronic infection; Epidemiological model; Malaria; Within host dynamics

Indexed keywords

DYNAMICS; MALARIA CONTROL;

CHRONIC INFECTION; EPIDEMIOLOGICAL MODELING; GENETIC DIVERSITY; INFECTION DYNAMICS; INFECTIOUS DISEASE; MALARIA; PLASMODIUM FALCIPARUM; PLAUSIBLE ASSUMPTIONS;

DISEASES;

CROSS REACTING ANTIBODY; CROSS REACTING ANTIGEN; ANTIGEN;

ANTIGENIC VARIATION; ARTICLE; CHRONIC DISEASE; CHRONICITY; DENSITY; DISEASE DURATION; HUMAN; MALARIA; MIXED INFECTION; NONHUMAN; PARASITE IMMUNITY; PARASITEMIA; THEORETICAL MODEL; ALGORITHM; ANIMAL; BLOOD; CHEMISTRY; COMPUTER SIMULATION; GENETICS; GENOTYPE; IMMUNE SYSTEM; MALARIA, FALCIPARUM; MARKOV CHAIN; PARASITOLOGY; PATHOGENICITY; PLASMODIUM FALCIPARUM; TIME FACTOR; TRANSMISSION;

PLASMODIUM FALCIPARUM;

ALGORITHMS; ANIMALS; ANTIGENS; COINFECTION; COMPUTER SIMULATION; GENOTYPE; HUMANS; IMMUNE SYSTEM; MALARIA, FALCIPARUM; MODELS, THEORETICAL; PLASMODIUM FALCIPARUM; STOCHASTIC PROCESSES; TIME FACTORS;

EID: 84923252859     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.1379     Document Type: Article

References (74)

1. WHO Malaria Report. 2012.
2. Bottius E, Guanzirolli A, Trape JF, Rogier C, Konate L, Druilhe P. 1996 Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction. Trans. R. Soc. Trop. Med. Hyg. 90, 15-19. (doi:10. 1016/S0035-9203(96) 90463-0)
3. Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, Joshi H. 2012 The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar. J. 11, 29. (doi:10. 1186/1475-2875-11-29)
4. Bowman NM et al. 2013 Comparative population structure of Plasmodium falciparum circumsporozoite protein NANP repeat lengths in Lilongwe, Malawi. Sci. Rep. 3, 1990. (doi:10. 1038/ srep01990)
5. Ross A, Koepfli C, Li X, Schoepflin S, Siba P, Mueller I, Felger I, Smith T. 2012 Estimating the numbers of malaria infections in blood samples using highresolution genotyping data. PLoS ONE 7, e42496. (doi:10. 1371/journal. pone. 0042496)
6. Nkhoma SC, Nair S, Cheeseman IH, Rohr-Allegrini C, Singlam S, Nosten F, Anderson TJ. 2012 Close kinship within multiple-genotype malaria parasite infections. Proc. R. Soc. B 279, 2589-2598. (doi:10. 1098/rspb. 2012. 0113)
7. Bousema T, Okell L, Felger I, Drakeley C. 2014 Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat. Rev. Microbiol. 12, 833-840. (doi:10. 1038/nrmicro3364)
8. Lin JT, Saunders DL, Meshnick SR. 2014 The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 30, 183-190. (doi:10. 1016/j. pt. 2014. 02. 004)
9. Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. 2013 The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev. Anti-Infect. Ther. 11, 623-639. (doi:10. 1586/eri. 13. 45)
10. McQueen PG, McKenzie FE. 2004 Age-structured red blood cell susceptibility and the dynamics of malaria infections. Proc. Natl Acad. Sci. USA 101, 9161-9166. (doi:10. 1073/pnas. 0308256101)
11. McQueen PG, McKenzie FE. 2008 Host control of malaria infections: constraints on immune and erythropoeitic response kinetics. PLoS Comput. Biol. 4, e1000149. (doi:10. 1371/journal. pcbi. 1000149)
12. McQueen PG, Williamson KC, McKenzie FE. 2013 Host immune constraints on malaria transmission: insights from population biology of within-host parasites. Malar. J. 12, 206. (doi:10. 1186/1475-2875-12-206)
13. Johnston GL, Smith DL, Fidock DA. 2013 Malaria's missing number: calculating the human component of R0 by a within-host mechanistic model of Plasmodium falciparum infection and transmission. PLoS Comput. Biol. 9, e1003025. (doi:10. 1371/ journal. pcbi. 1003025)
14. Killeen GF, Ross A, Smith T. 2006 Infectiousness of malaria-endemic human populations to vectors. Am. J. Trop. Med. Hyg. 75(2 Suppl.), 38-45.
15. Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L. 2006 A model for natural immunity to asexual blood stages of Plasmodium falciparum malaria in endemic areas. Am. J. Trop. Med. Hyg. 75(2 Suppl.), 19-31.
16. Smith T et al. 2006 Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am. J. Trop. Med. Hyg. 75(2 Suppl.), 1-10.
17. Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M. 2006 Relationship between the entomologic inoculation rate and the force of infection for Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 75(2 Suppl.), 11-18.
18. Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L. 2006 An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am. J. Trop. Med. Hyg. 75(2 Suppl.), 56-62.
19. Felger I, Maire M, Bretscher MT, Falk N, Tiaden A, Sama W, Beck HP, Owusu-Agyei S, Smith TA. 2012 The dynamics of natural Plasmodium falciparum infections. PLoS ONE 7, e45542. (doi:10. 1371/ journal. pone. 0045542)
20. Molineaux L, Gramiccia G. 1980 The Garki project. Geneva, The switzerland: World Health Organization.
21. Bretscher MT, Maire N, Chitnis N, Felger I, Owusu-Agyei S, Smith T. 2011 The distribution of Plasmodium falciparum infection durations. Epidemics 3, 109-118. (doi:10. 1016/j. epidem. 2011. 03. 002)
22. Ferguson N, Anderson R, Gupta S. 1999 The effect of antibody-dependent enhancement on the transmission dynamics and persistence of multiplestrain pathogens. Proc. Natl Acad. Sci. USA 96, 790-794. (doi:10. 1073/pnas. 96. 2. 790)
23. Gupta S, Ferguson N, Anderson R. 1998 Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. Science 280, 912-915. (doi:10. 1126/science. 280. 5365. 912)
24. Gupta S, Maiden MC, Feavers IM, Nee S, May RM, Anderson RM. 1996 The maintenance of strain structure in populations of recombining infectious agents. Nat. Med. 2, 437-442. (doi:10. 1038/ nm0496-437)
25. Buckee C, Danon L, Gupta S. 2007 Host community structure and the maintenance of pathogen diversity. Proc. R. Soc. B 274, 1715-1721. (doi:10. 1098/rspb. 2007. 0415)
26. Buckee CO, Koelle K, Mustard MJ, Gupta S. 2004 The effects of host contact network structure on pathogen diversity and strain structure. Proc. Natl Acad. Sci. USA 101, 10 839-10 844. (doi:10. 1073/ pnas. 0402000101)
27. Buckee CO, Recker M, Watkins ER, Gupta S. 2011 Role of stochastic processes in maintaining discrete strain structure in antigenically diverse pathogen populations. Proc. Natl Acad. Sci. USA 108, 15 504-15 509. (doi:10. 1073/pnas. 1102445108)
28. Koella JC. 1991 On the use of mathematical models of malaria transmission. Acta Trop. 49, 1-25. (doi:10. 1016/0001-706X(91)90026-G)
29. Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. 2012 Ross, Macdonald, and a theory for the dynamics and control of mosquitotransmitted pathogens. PloS Pathog. 8, e1002588. (doi:10. 1371/journal. ppat. 1002588)
30. Eckhoff P. 2012 P. falciparum infection durations and infectiousness are shaped by antigenic variation and innate and adaptive host immunity in a mathematical model. PloS ONE 7, e44950. (doi:10. 1371/journal. pone. 0044950)
31. Hoshen MB, Heinrich R, Stein WD, Ginsburg H. 2000 Mathematical modelling of the withinhost dynamics of Plasmodium falciparum. Parasitology 121, 227-235. (doi:10. 1017/S00311 82099006368)
32. Klein EY, Graham AL, Llinas M, Levin S. 2014 Crossreactive immune responses as primary drivers of malaria chronicity. Infect. Immun. 82, 140-151. (doi:10. 1128/IAI. 00958-13)
33. Johnson PL, Kochin BF, Ahmed R, Antia R. 2012 How do antigenically varying pathogens avoid cross-reactive responses to invariant antigens? Proc. R. Soc. B 279, 2777-2785. (doi:10. 1098/rspb. 2012. 0005)
34. Eichner M, Diebner HH, Molineaux L, Collins WE, Jeffery GM, Dietz K. 2001 Genesis, sequestration and survival of Plasmodium falciparum gametocytes: parameter estimates from fitting a model to malariatherapy data. Trans. R. Soc Trop. Med. Hyg. 95, 497-501. (doi:10. 1016/S0035-9203(01) 90016-1)
35. Molineaux L, Diebner HH, Eichner M, Collins WE, Jeffery GM, Dietz K. 2001 Plasmodium falciparum parasitaemia described by a new mathematical model. Parasitology 122, 379-391.
36. Recker M, Al-Bader R, Gupta S. 2005 A mathematical model for a new mechanism of phenotypic variation in malaria. Parasitology 131, 151-159. (doi:10. 1017/S0031182005007481)
37. Recker M, Buckee CO, Serazin A, Kyes S, Pinches R, Christodoulou Z, Springer AL, Gupta S, Newbold CI. 2011 Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PloS Pathog. 7, e1001306. (doi:10. 1371/ journal. ppat. 1001306)
38. Recker M, Gupta S. 2006 Conflicting immune responses can prolong the length of infection in Plasmodium falciparum malaria. Bull. Math. Biol. 68, 821-835. (doi:10. 1007/s11538-005-9041-0)
39. Recker M, Nee S, Bull PC, Kinyanjui S, Marsh K, Newbold C, Gupta S. 2004 Transient cross-reactive immune responses can orchestrate antigenic variation in malaria. Nature 429, 555-558. (doi:10. 1038/nature02486)
40. McKenzie FE, Bossert WH. 2005 An integrated model of Plasmodium falciparum dynamics. J. Theor. Biol. 232, 411-426. (doi:10. 1016/j. jtbi. 2004. 08. 021)
41. Collins WE, Jeffery GM. 1999 A retrospective examination of the patterns of recrudescence in patients infected with Plasmodium falciparum. Am. J. Trop. Med. Hyg. 61(1 Suppl.), 44-48. (doi:10. 4269/tropmed. 1999. 61-044)
42. Simpson JA, Aarons L, Collins WE, Jeffery GM, White NJ. 2002 Population dynamics of untreated Plasmodium falciparum malaria within the adult human host during the expansion phase of the infection. Parasitology 124, 247-263.
43. Antia R, Yates A, de Roode JC. 2008 The dynamics of acute malaria infections. I. Effect of the parasite's red blood cell preference. Proc. R. Soc. B 275, 1449-1458. (doi:10. 1098/rspb. 2008. 0198)
44. Newbold CI, Craig AG, Kyes S, Berendt AR, Snow RW, Peshu N, Marsh K. 1997 PfEMP1, polymorphism and pathogenesis. Ann. Trop. Med. Parasitol. 91, 551-557. (doi:10. 1080/00034989760923)
45. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH. 1995 Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82, 101-110. (doi:10. 1016/0092-8674(95)90056-X)
46. Dzikowski R, Templeton TJ, Deitsch K. 2006 Variant antigen gene expression in malaria. Cell. Microbiol. 8, 1371-1381. (doi:10. 1111/j. 1462-5822. 2006. 00760. x)
47. Bull PC, Lowe BS, Kortok M, Marsh K. 1999 Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect. Immun. 67, 733-739.
48. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. 1998 Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 4, 358-360. (doi:10. 1038/nm0398-358)
49. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ. 1995 Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82, 77-87. (doi:10. 1016/0092-8674(95)90054-3)
50. Claessens A, Hamilton WL, Kekre M, Otto TD, Faizullabhoy A, Rayner JC, Kwiatkowski D. 2014 Generation of antigenic diversity in Plasmodium falciparum by structured rearrangement of var genes during mitosis. PLoS Genet. 10, e1004812. (doi:10. 1371/journal. pgen. 1004812).
51. Dzikowski R, Frank M, Deitsch K. 2006 Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLoS Pathog. 2, e22. (doi:10. 1371/ journal. ppat. 0020022)
52. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M. 1998 Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17, 5418-5426. (doi:10. 1093/emboj/17. 18. 5418)
53. Dzikowski R, Li F, Amulic B, Eisberg A, Frank M, Patel S, Wellems TE, Deitsch KW. 2007 Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep. 8, 959-965. (doi:10. 1038/sj. embor. 7401063)
54. Enderes C, Kombila D, Dal-Bianco M, Dzikowski R, Kremsner P, Frank M. 2011 Var gene promoter activation in clonal Plasmodium falciparum isolates follows a hierarchy and suggests a conserved switching program that is independent of genetic background. J. Infect. Dis. 204, 1620-1631. (doi:10. 1093/infdis/jir594)
55. Bachmann A, Predehl S, May J, Harder S, Burchard GD, Gilberger TW, Tannich E, Bruchhaus I. 2011 Highly coordinated var gene expression and switching in clinical Plasmodium falciparum isolates from non-immune malaria patients. Cell. Microbiol. 13, 1397-1409. (doi:10. 1111/j. 1462-5822. 2011. 01629. x)
56. Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI. 2004 Variable var transition rates underlie antigenic variation in malaria. Proc. Natl Acad. Sci. USA 101, 11 129-11 134. (doi:10. 1073/ pnas. 0402347101)
57. White NJ. 2014 Malaria: a molecular marker of artemisinin resistance. Lancet 383, 1439-1440. (doi:10. 1016/S0140-6736(14)60656-5)
58. Roberts DJ, Craig AG, Berendt AR, Pinches R, Nash G, Marsh K, Newbold CI. 1992 Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature 357, 689-692. (doi:10. 1038/ 357689a0)
59. Noble R, Christodoulou Z, Kyes S, Pinches R, Newbold CI, Recker M. 2013 The antigenic switching network of Plasmodium falciparum and its implications for the immuno-epidemiology of malaria. eLife 2, e01074. (doi:10. 7554/ eLife. 01074)
60. Fastman Y, Noble R, Recker M, Dzikowski R. 2012 Erasing the epigenetic memory and beginning to switch: the onset of antigenic switching of var genes in Plasmodium falciparum. PLoS ONE 7, e34168. (doi:10. 1371/journal. pone. 0034168)
61. Murphy K, Travers P, Walport M, Janeway C. 2012 Janeway's immunobiology, 8th edn, p. 868. New York: Garland Science.
62. Stein M. 1987 Large sample properties of simulations using latin hypercube sampling. Technometrics 29, 143-151. (doi:10. 1080/ 00401706. 1987. 10488205)
63. Miller LH, Good MF, Milon G. 1994 Malaria pathogenesis. Science 264, 1878-1883. (doi:10. 1126/science. 8009217)
64. Jakeman GN, Saul A, Hogarth WL, Collins WE. 1999 Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119, 127-133. (doi:10. 1017/S0031182099004564)
65. Scherf A, Lopez-Rubio JJ, Riviere L. 2008 Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62, 445-470. (doi:10. 1146/annurev. micro. 61. 080706. 093134)
66. Wunderlich G, Alves FP, Golnitz U, Tada MS, Camargo EF, Pereira-da-Silva LH. 2005 Rapid turnover of Plasmodium falciparum var gene transcripts and genotypes during natural nonsymptomatic infections. Revista do Instituto de Medicina Tropical de Sao Paulo 47, 195-201. (doi:10. 1590/S0036-46652005000400004)
67. Blomqvist K et al. 2010 var gene transcription dynamics in Plasmodium falciparum patient isolates. Mol. Biochem. Parasitol. 170, 74-83. (doi:10. 1016/ j. molbiopara. 2009. 12. 002)
68. Severins M, Klinkenberg D, Heesterbeek H. 2012 How selection forces dictate the variant surface antigens used by malaria parasites. J. R. Soc. Interface 9, 246-260. (doi:10. 1098/rsif. 2011. 0239)
69. Lavstsen T, Magistrado P, Hermsen CC, Salanti A, Jensen AT, Sauerwein R, Hviid L, Theander TG, Staalsoe T. 2005 Expression of Plasmodium falciparum erythrocyte membrane protein 1 in experimentally infected humans. Malar. J. 4, 21. (doi:10. 1186/1475-2875-4-21)
70. Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, Lavstsen T. 2009 The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol. Int. 58, 478-480. (doi:10. 1016/j. parint. 2009. 07. 004)
71. Warimwe GM, Recker M, Kiragu EW, Buckee CO, Wambua J, Musyoki JN, Marsh K, Bull PC. 2013 Plasmodium falciparum var gene expression homogeneity as a marker of the host-parasite relationship under different levels of naturally acquired immunity to malaria. PLoS ONE 8, e70467. (doi:10. 1371/journal. pone. 0070467)
72. Lau CK et al. 2014 Structural conservation despite huge sequence diversity allows EPCR binding by the PfEMP1 family implicated in severe childhood malaria. Cell Host Microb. (doi:10. 1016/j. chom. 2014. 11. 007)
73. Gitau EN et al. 2014 CD4 T cell responses to the Plasmodium falciparum erythrocyte membrane protein 1 in children with mild malaria. J. Immunol. 192, 1753-1761. (doi:10. 4049/ jimmunol. 1200547)
74. Albrecht L, Angeletti D, Moll K, Blomqvist K, Valentini D, D'Alexandri FL, Maurer M, Wahlgren M. 2014 B-cell epitopes in NTS-DBL1alpha of PfEMP1 recognized by human antibodies in rosetting Plasmodium falciparum. PLoS ONE 9, e113248. (doi:10. 1371/journal. pone. 0113248)