Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model

A striking feature of lymphatic filariasis is the considerable heterogeneity in infection burden observed between hosts, which greatly complicates the analysis of the population dynamics of the disease. Here, we describe the first application of the moment closure equation approach to model the sour...

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Veröffentlicht in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 1998-01, Vol.265 (1391), p.155-165
Hauptverfasser: Michael, E., Grenfell, B. T., Isham, V. S., Denham, D. A., Bundy, D. A. P.
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container_start_page 155
container_title Proceedings of the Royal Society. B, Biological sciences
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creator Michael, E.
Grenfell, B. T.
Isham, V. S.
Denham, D. A.
Bundy, D. A. P.
description A striking feature of lymphatic filariasis is the considerable heterogeneity in infection burden observed between hosts, which greatly complicates the analysis of the population dynamics of the disease. Here, we describe the first application of the moment closure equation approach to model the sources and the impact of this heterogeneity for macrofilarial population dynamics. The analysis is based on the closest laboratory equivalent of the life cycle and immunology of infection in humans-cats chronically infected with the filarial nematode Brugia pahangi. Two sets of long-term experiments are analysed: hosts given either single primary infections or given repeat infections. We begin by quantifying changes in the mean and aggregation of adult parasites (inversely measured by the negative binomial parameter,k in cohorts of hosts using generalized linear models. We then apply simple stochastic models to interpret observed patterns. The models and empirical data indicate that parasite aggregation tracks the decline in the mean burden with host age in primary infections. Conversely, in repeat infections, aggregation increases as the worm burden declines with experience of infection. The results show that the primary infection variability is consistent with heterogeneities in parasite survival between hosts. By contrast, the models indicate that the reduction in parasite variability with time in repeat infections is most likely due to the 'filtering' effect of a strong, acquired immune response, which gradually acts to remove the initial variability generated by heterogeneities in larval mortality. We discuss this result in terms of the homogenizing effect of host immunity-driven density-dependence on macrofilarial burden in older hosts.
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By contrast, the models indicate that the reduction in parasite variability with time in repeat infections is most likely due to the 'filtering' effect of a strong, acquired immune response, which gradually acts to remove the initial variability generated by heterogeneities in larval mortality. We discuss this result in terms of the homogenizing effect of host immunity-driven density-dependence on macrofilarial burden in older hosts.</description><subject>Aggregation</subject><subject>animal parasitic nematodes</subject><subject>Animals</subject><subject>Brugia pahangi</subject><subject>Cat Diseases - immunology</subject><subject>Cat Diseases - parasitology</subject><subject>Cats</subject><subject>Elephantiasis, Filarial - immunology</subject><subject>Elephantiasis, Filarial - parasitology</subject><subject>Elephantiasis, Filarial - veterinary</subject><subject>Filarial elephantiasis</subject><subject>Filariasis</subject><subject>Heterogeneity</subject><subject>Host-Parasite Interactions</subject><subject>host-parasite relationships</subject><subject>Immunity</subject><subject>Infections</subject><subject>Larvae</subject><subject>Macrofilarial Dynamics</subject><subject>Modeling</subject><subject>Models, Biological</subject><subject>Models, Statistical</subject><subject>Moment Closure Equations</subject><subject>Mortality</subject><subject>Parasite hosts</subject><subject>Parasite Immunity</subject><subject>Parasites</subject><subject>Parasitology</subject><subject>simulation models</subject><issn>0962-8452</issn><issn>1471-2954</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UbuO1DAUjRBoWRZaCiREKroMdh5-UIBgxWu1iAKW9sqxncRDEgc7WcjfYyujEVNAZV2fh4_vSZLHGO0w4uyF81O9w5yzHcopvZOc45LiLOdVeTc5R5zkGSur_H7ywPs9QohXrDpLznhJS8rZeaI_W6X73oxteiucEbXpzbymZkz7dZg6MRuZNqaPkDf-ZToI6ezhok_VOorBSB_5c6fTt25pjUgn0YmxNZkUczpE_4fJvUb0Xj86nBfJzft33y4_ZtdfPny6fHOdSYLYnEmlVakErWtFSt7UMW0efqWQFogQVCnJGK8JU0LkhRS64A3TFLOKa6UwLy6SV5vvtNSDVlKPsxM9TM4Mwq1ghYFTZDQdtPYWMGGMkTwYPD8YOPtz0X6GwXgZFiRGbRcPlBNe8rIMxN1GDOvw3unm-AhGEIuBWAzEYiAWEwRP_452pB-aCHix4c6uYUVWGj2vsLeLG8P4b9cnm2rvZ-uOphXivApgtoHGz_r3ERTuBxBa0Aq-sxIKyq8wuyIQ-Xjjd6btfhmn4SRLGCbna8hJBbjgGHAVNa__q4lxpR3nsO8TITRLH4pRTXB4tjk0woJonfFw8zVHuEA5o0UotfgD8Svotw</recordid><startdate>19980122</startdate><enddate>19980122</enddate><creator>Michael, E.</creator><creator>Grenfell, B. 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P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model</atitle><jtitle>Proceedings of the Royal Society. B, Biological sciences</jtitle><addtitle>Proc Biol Sci</addtitle><date>1998-01-22</date><risdate>1998</risdate><volume>265</volume><issue>1391</issue><spage>155</spage><epage>165</epage><pages>155-165</pages><issn>0962-8452</issn><eissn>1471-2954</eissn><abstract>A striking feature of lymphatic filariasis is the considerable heterogeneity in infection burden observed between hosts, which greatly complicates the analysis of the population dynamics of the disease. Here, we describe the first application of the moment closure equation approach to model the sources and the impact of this heterogeneity for macrofilarial population dynamics. 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By contrast, the models indicate that the reduction in parasite variability with time in repeat infections is most likely due to the 'filtering' effect of a strong, acquired immune response, which gradually acts to remove the initial variability generated by heterogeneities in larval mortality. We discuss this result in terms of the homogenizing effect of host immunity-driven density-dependence on macrofilarial burden in older hosts.</abstract><cop>England</cop><pub>The Royal Society</pub><pmid>9474798</pmid><doi>10.1098/rspb.1998.0277</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record>
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ispartof Proceedings of the Royal Society. B, Biological sciences, 1998-01, Vol.265 (1391), p.155-165
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subjects Aggregation
animal parasitic nematodes
Animals
Brugia pahangi
Cat Diseases - immunology
Cat Diseases - parasitology
Cats
Elephantiasis, Filarial - immunology
Elephantiasis, Filarial - parasitology
Elephantiasis, Filarial - veterinary
Filarial elephantiasis
Filariasis
Heterogeneity
Host-Parasite Interactions
host-parasite relationships
Immunity
Infections
Larvae
Macrofilarial Dynamics
Modeling
Models, Biological
Models, Statistical
Moment Closure Equations
Mortality
Parasite hosts
Parasite Immunity
Parasites
Parasitology
simulation models
title Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model
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