×

How does within-host dynamics affect population-level dynamics? Insights from an immuno-epidemiological model of malaria. (English) Zbl 1383.92078

Summary: Malaria is one of the most common mosquito-borne diseases widespread in the tropical and subtropical regions. Few models coupling the within-host malaria dynamics with the between-host mosquito-human dynamics have been developed. In this paper, by adopting the nested approach, a malaria transmission model with immune response of the host is formulated. Applying age-structured partial differential equations for the between-host dynamics, we describe the asymptomatic and symptomatic infectious host population for malaria transmission. The basic reproduction numbers for the within-host model and for the coupled system are derived, respectively. The existence and stability of the equilibria of the coupled model are analyzed. We show numerically that the within-host model can exhibit complex dynamical behavior, possibly even chaos. In contrast, equilibria in the immuno-epidemiological model are globally stable and their stabilities are determined by the reproduction number. Increasing the activation rate of the within-host immune response “dampens” the sensitivity of the population level reproduction number and prevalence to the increase of the within-host reproduction of the pathogen. From public health perspective this means that treatment in a population with higher immunity has less impact on the population-level reproduction number and prevalence than in a population with less immunity.

MSC:

92D30 Epidemiology
92D40 Ecology
Full Text: DOI

References:

[1] OaksSC Jr, MitchellVS, PearsonGW, CarpenterCCJ, eds. Malaria Obstacle and Opportunities. National Academy: Washington D.C., 1991.
[2] WHO, World Malaria Report(205). http://www.who.int/malaria/publications/world-malaria-report-2015/en/. Accessed March 1, 2015.
[3] RaghavendraK, BarikTK, ReddyBPN, SharmaP, DashAP. Malaria vector control: from past to future. Parasitol Res. 2011;108:757‐779.
[4] LindbladeKA, SteinhardtL, SamuelsA, KachurSP, SlutskerL. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11(6):623‐639.
[5] http://www.cdc.gov/malaria/about/disease.html. Accessed February 1, 2015.
[6] GalatasB, BassatQ, MayorA. Malaria parasites in the asymptomatic: looking for the hay in the Haystack. Trends Parasitol. 2016;32(4):296‐308.
[7] NigerAM, GumelAB. Mathematical analysis of the role of repeated exposure on malaria transmission dynamics. Different Equat Dyna Syst. 2008;16(3):251‐287. · Zbl 1181.34056
[8] BousemaT, OkellL, FelgerI, DrakeleyC. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833‐840.
[9] RossR. The Prevention of Malaria. 2nd edn. John Murray: London, 1911.
[10] CaiL, MartchevaM, LiX. Competitive exclusion in a vector‐host epidemic model with distributed delay. J Biol Dyn. 2013;7(1):47‐67. · Zbl 1448.92280
[11] CaiL‐M, LiX‐Z, FangB, RuanS. Global properties of vector‐host disease models with time delays. J Math Biol. 2017;74:1397‐1423. · Zbl 1403.92287
[12] MandalS, Rup SarkarR, SinhaS. Mathematical models of malaria—a review. Malaria J. 2011;10:202.
[13] ReinerRC, PerkinsTA, BarkerCM, Fernando ChavesL, EllisAM, GeorgeDB, Le MenachA, PulliamJRC, BisanzioD, BuckeeC, ChiyakaC, CummingsDAT, GarciaAJ, GattonML, GethingPW, HartleyDM, JohnstonG, KleinEY, MichaelE, LindsaySW, LloydAL, PigottDM, ReisenWK, RuktanonchaiN, SinghBK, TatemAJ, KitronU, HaySI, ScottTW, SmithDL. A systematic review of mathematical models of mosquito‐borne pathogen transmission: 1970‐2010. J R Soc Interface. 2013;10:1‐1320120921.
[14] RuanS, XiaoD, BeierJC. On the delayed Ross‐Macdonald model for malaria transmission. Bull Math Biol. 2008;70:1098‐1114. · Zbl 1142.92040
[15] ProsperO, MartchevaM. Impact of enhanced malaria control on the competition between plasmodium falciparum and plasmodium vivax in India. Math Biosc. 2013;242:33‐50. · Zbl 1316.92090
[16] LiJ. A malaria model with partial immunity in humans. Math Biosci Eng. 2008;5(4):789‐801. · Zbl 1171.34032
[17] InabaH, SekineH. A mathematical model for Chagas disease with infection‐age‐dependent infectivity. Math Biosci. 2004;190:39‐69. · Zbl 1049.92033
[18] Vargas‐De‐LeonC, EstevaL, KorobeinikovA. Age‐dependency in host‐vector models: the global analysis. Appl Math Comput. 2014;243:969‐981. · Zbl 1335.92104
[19] LangeA, FergusonNM. Antigenic diversity, transmission mechanisms, and the evolution of pathogens. PLoS Comput Biol. 2009;5:e1000536.
[20] GoodMF, XuH, WykesM, EngwerdaCR. Development and regulation of cell‐ mediated immune responses to the blood stages of malaria: implications from vaccine reasearch, Annu. Rev Immunol. 2005;23:69‐99.
[21] HellriegelB. Immunoepidemiology‐bridging the gap between immunology epidemiology. Trends Paras. 2001;17:102‐106.
[22] GilchristMA, SasakiA. Modeling host‐parasite coevolution: a nested approach based on mechanistic models. J Theor Biol. 2002;218:289‐308.
[23] GulbudakH, CannataroV, TuncerN, MartchevaM. Vector‐borne pathogen and host evolution in a structured immuno‐epidemiological system. Bull Math Biol. 2017;79(2):325‐355. · Zbl 1366.92122
[24] MartchevaM, TuncerN, St MaryC. Coupling within‐host and between‐host infectious diseases models. Biomath. 2015;4(2):1510091. · Zbl 1368.92188
[25] MartchevaM, LenhartS, EdaS, KlinkenbergD, MonotaniE, StabelJ. An immuno‐epidemiological model of Johne’s disease in cattle. Vet Res. 2015;46:69‐81.
[26] MartchevaM, LiX. Linking immunological and epidemiological dynamics of HIV: the case of super‐infection. J Biol Dyn. 2013;7(1):161-182. · Zbl 1447.92451
[27] ShenM, XiaoY, RongL. Global stability of an infection‐age structured HIV‐1 model linking within‐host and between‐host dynamics. Math Biosci. 2015;263:37‐50. · Zbl 1371.92130
[28] LegrosM, BonhoefferS. A combined within‐host and between‐hosts modelling framework for the evolution of resistance to antimalarial drugs. J R Soc Interface. 2016;13:1‐10:20160148.
[29] ChurcherTS, SindenRE, et al. Probability of transmission of malaria fromm mosquito to human is regulated by mosquito parasite density in naive and vaccinated hosts. PLoS Pathog. 2017;13(1):1‐18;e100.
[30] BatistaElisPA, CostaElizangelaFM, SilvaAlexandreA. Anopheles darlingi (Diptera: Culicidae) displays increased attractiveness to infected individuals with Plasmodium vivax gametocytes. Parasit Vectors. 2014;7:251‐254.
[31] TuncerN, GulbudakH, CannataroVL, MartchevaM. Structural and practical identifiability issues of immuno‐epidemiological vector host models with application to Rift Valley fever. Bull Math Biol. 2016;78(9):1796‐1827. · Zbl 1352.92173
[32] NeblT, De VeerMJ, SchofieldL. Stimulation of innate immune responses by malarial glycosylphosphatidylinositol via pattern recognition receptors. Parasitology. 2005;130:S45‐S62.
[33] McQueenPG, WilliamsonKC, McKenzieFE. Host immune constraints on malaria transmission: insights from population biology of within‐host parasites. Malaria J. 2013;12:206‐223.
[34] AndersonRM. Complex dynamics behaviors in the interaction between parasite populations and the host’s immune system. Int J Parasitol. 1998;28:55‐566.
[35] AntiaR, LevinBR, MayRM. Within‐host population dynamics and the evolution and maintenance of microparasite virulence. Am Nat. 1994;144(3):457‐472.
[36] LiY, RuanS, XiaoD. The within‐host dynamics of malaria infection with immune response. Math Biosci Eng. 2011;8(4):999‐1018. · Zbl 1259.34027
[37] TumwiineJ, MugishaJYT, LuboobiLS. On global stablity of the intra‐host dynamics of malaria and the immune system. J Math Anal Appl. 2008;341:855‐869. · Zbl 1132.92010
[38] CaiL, MartchevaM, LiX. Epidemic models with age of infection, indirect transmission and incomplete treatment. Discrete Cont Dyn‐B. 2013;18:2239‐2265. · Zbl 1277.92021
[39] MagalP, McCluskeyCC, WebbGF. Liapunov functional and global asymptotic stability for an infection‐age model. Appl Anal. 2010;89:1109‐1140. · Zbl 1208.34126
[40] DiekmannO, HeesterbeekJAP, MetzJAJ. On the definition and computation of the basic reproduction ratio in models for infectious diseases in heterogeneous populations. J Math Biol. 1990;28:365‐382. · Zbl 0726.92018
[41] HuangG, LiuX, TakeuchiY. Lyapunov functions and global stability for age‐structured HIV infection model. SIAM J Appl Math. 2012;72(1):25‐38. · Zbl 1238.92032
[42] BrauerF, ShuaiZ, van denDriesscheP. Dynamics of an age‐of‐infection cholera model. Math Biosci Eng. 2013;10:1335‐1349. · Zbl 1273.92050
[43] McCluskeyCC. Complete global stability for an SIR epidemic model with delay‐distributed or discrete. Nonlinear Anal: Real World Appl.2010;11:55‐59. · Zbl 1185.37209
[44] ShuaiZ, van denDriesscheP. Global stability of infectious disease model using Lyapunov functions. SIAM J Appl Math. 2013;73:1513‐1532. · Zbl 1308.34072
[45] MartchevaM, LiX. Competitive exclusion in an infection‐age structured model with environmental transmission. J Math Anal Appl. 2013;408:225‐246. · Zbl 1306.92047
[46] HirshWM, HanishH, GabrielJP. Differential equation model of some parasitic infections: methods for the study of asymptotic behavior. Comm Pure Appl Math. 1985;38:733‐753. · Zbl 0637.92008
[47] MartchevaM, ThiemeHR. Progression‐age enhanced backward bifurcation in an epidemic model with super‐infection. J Math Biol. 2003;46:385‐424. · Zbl 1097.92046
[48] ThiemeHR. Uniform persistence for non‐autonomous semiflows in population biology. Math Biosci. 2000;166:173‐201. · Zbl 0970.37061
[49] TumwiineJ, LuckhausS, MugishaJYT, LuboobiLS. An age‐structured mathematical model for the within host dynamics of malaria and the immune system. J Math Model Algor. 2008;7:79‐97. · Zbl 1132.92016
[50] Malaria Vaccines. http://web.stanford.edu/class/humbio153/MalariaVac/index.html. Accessed December 20, 2015.
[51] MartiM, BaumJ, RugM, CowmanAF. Signal‐mediated export of proteins from the malaria parasite to the host erythrocyte. J Cell Biol. 2005;171(4):587‐592.
[52] Life expectancy at birth, total (years), World Bank Data. http://data.worldbank.org/indicator/SP.DYN.LE00.IN. 2016
[53] MartchevaM, HoppensteadtF. India’s approach to elliminating plasmodium falciparum malaria: a modeling perspective. J Biol Systems. 2010;18(4):867‐891. · Zbl 1404.92195
[54] ChenI, ClarkeSE, GoslingR, HamainzaB, KilleenG, MagillA, O’MearaW, PriceRN, RileyEM. Asymptomatical malaria: a chronic and debilitating infection that should be treated. PLoS Med. 2016;13(1):e1001942.
[55] https://en.wikipedia.org/wiki/Anopheles. Accessed October 2, 2015.
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.