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...
Gespeichert in:
Veröffentlicht in: | Proceedings of the Royal Society. B, Biological sciences Biological sciences, 1998-01, Vol.265 (1391), p.155-165 |
---|---|
Hauptverfasser: | , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 165 |
---|---|
container_issue | 1391 |
container_start_page | 155 |
container_title | Proceedings of the Royal Society. B, Biological sciences |
container_volume | 265 |
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. |
doi_str_mv | 10.1098/rspb.1998.0277 |
format | Article |
fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_1688862</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>50995</jstor_id><sourcerecordid>50995</sourcerecordid><originalsourceid>FETCH-LOGICAL-c608t-cded4da7bbd649fb09582277d0ea06605dc889b68daa23cae39f8e71859edd193</originalsourceid><addsrcrecordid>eNp9UbuO1DAUjRBoWRZaCiREKroMdh5-UIBgxWu1iAKW9sqxncRDEgc7WcjfYyujEVNAZV2fh4_vSZLHGO0w4uyF81O9w5yzHcopvZOc45LiLOdVeTc5R5zkGSur_H7ywPs9QohXrDpLznhJS8rZeaI_W6X73oxteiucEbXpzbymZkz7dZg6MRuZNqaPkDf-ZToI6ezhok_VOorBSB_5c6fTt25pjUgn0YmxNZkUczpE_4fJvUb0Xj86nBfJzft33y4_ZtdfPny6fHOdSYLYnEmlVakErWtFSt7UMW0efqWQFogQVCnJGK8JU0LkhRS64A3TFLOKa6UwLy6SV5vvtNSDVlKPsxM9TM4Mwq1ghYFTZDQdtPYWMGGMkTwYPD8YOPtz0X6GwXgZFiRGbRcPlBNe8rIMxN1GDOvw3unm-AhGEIuBWAzEYiAWEwRP_452pB-aCHix4c6uYUVWGj2vsLeLG8P4b9cnm2rvZ-uOphXivApgtoHGz_r3ERTuBxBa0Aq-sxIKyq8wuyIQ-Xjjd6btfhmn4SRLGCbna8hJBbjgGHAVNa__q4lxpR3nsO8TITRLH4pRTXB4tjk0woJonfFw8zVHuEA5o0UotfgD8Svotw</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>79694944</pqid></control><display><type>article</type><title>Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model</title><source>MEDLINE</source><source>Jstor Complete Legacy</source><source>PubMed Central</source><creator>Michael, E. ; Grenfell, B. T. ; Isham, V. S. ; Denham, D. A. ; Bundy, D. A. P.</creator><creatorcontrib>Michael, E. ; Grenfell, B. T. ; Isham, V. S. ; Denham, D. A. ; Bundy, D. A. P.</creatorcontrib><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.</description><identifier>ISSN: 0962-8452</identifier><identifier>EISSN: 1471-2954</identifier><identifier>DOI: 10.1098/rspb.1998.0277</identifier><identifier>PMID: 9474798</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>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</subject><ispartof>Proceedings of the Royal Society. B, Biological sciences, 1998-01, Vol.265 (1391), p.155-165</ispartof><rights>Copyright 1998 The Royal Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c608t-cded4da7bbd649fb09582277d0ea06605dc889b68daa23cae39f8e71859edd193</citedby><cites>FETCH-LOGICAL-c608t-cded4da7bbd649fb09582277d0ea06605dc889b68daa23cae39f8e71859edd193</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/50995$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/50995$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,728,781,785,804,886,27929,27930,53796,53798,58022,58255</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9474798$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Michael, E.</creatorcontrib><creatorcontrib>Grenfell, B. T.</creatorcontrib><creatorcontrib>Isham, V. S.</creatorcontrib><creatorcontrib>Denham, D. A.</creatorcontrib><creatorcontrib>Bundy, D. A. P.</creatorcontrib><title>Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model</title><title>Proceedings of the Royal Society. B, Biological sciences</title><addtitle>Proc Biol Sci</addtitle><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.</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. T.</creator><creator>Isham, V. S.</creator><creator>Denham, D. A.</creator><creator>Bundy, D. A. P.</creator><general>The Royal Society</general><scope>FBQ</scope><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19980122</creationdate><title>Modelling variability in lymphatic filariasis: macrofilarial dynamics in the Brugia pahangi-cat model</title><author>Michael, E. ; Grenfell, B. T. ; Isham, V. S. ; Denham, D. A. ; Bundy, D. A. P.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c608t-cded4da7bbd649fb09582277d0ea06605dc889b68daa23cae39f8e71859edd193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>Aggregation</topic><topic>animal parasitic nematodes</topic><topic>Animals</topic><topic>Brugia pahangi</topic><topic>Cat Diseases - immunology</topic><topic>Cat Diseases - parasitology</topic><topic>Cats</topic><topic>Elephantiasis, Filarial - immunology</topic><topic>Elephantiasis, Filarial - parasitology</topic><topic>Elephantiasis, Filarial - veterinary</topic><topic>Filarial elephantiasis</topic><topic>Filariasis</topic><topic>Heterogeneity</topic><topic>Host-Parasite Interactions</topic><topic>host-parasite relationships</topic><topic>Immunity</topic><topic>Infections</topic><topic>Larvae</topic><topic>Macrofilarial Dynamics</topic><topic>Modeling</topic><topic>Models, Biological</topic><topic>Models, Statistical</topic><topic>Moment Closure Equations</topic><topic>Mortality</topic><topic>Parasite hosts</topic><topic>Parasite Immunity</topic><topic>Parasites</topic><topic>Parasitology</topic><topic>simulation models</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Michael, E.</creatorcontrib><creatorcontrib>Grenfell, B. T.</creatorcontrib><creatorcontrib>Isham, V. S.</creatorcontrib><creatorcontrib>Denham, D. A.</creatorcontrib><creatorcontrib>Bundy, D. A. P.</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the Royal Society. B, Biological sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Michael, E.</au><au>Grenfell, B. T.</au><au>Isham, V. S.</au><au>Denham, D. A.</au><au>Bundy, D. A. 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. 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.</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> |
fulltext | fulltext |
identifier | ISSN: 0962-8452 |
ispartof | Proceedings of the Royal Society. B, Biological sciences, 1998-01, Vol.265 (1391), p.155-165 |
issn | 0962-8452 1471-2954 |
language | eng |
recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_1688862 |
source | MEDLINE; Jstor Complete Legacy; PubMed Central |
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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-12T09%3A18%3A21IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Modelling%20variability%20in%20lymphatic%20filariasis:%20macrofilarial%20dynamics%20in%20the%20Brugia%20pahangi-cat%20model&rft.jtitle=Proceedings%20of%20the%20Royal%20Society.%20B,%20Biological%20sciences&rft.au=Michael,%20E.&rft.date=1998-01-22&rft.volume=265&rft.issue=1391&rft.spage=155&rft.epage=165&rft.pages=155-165&rft.issn=0962-8452&rft.eissn=1471-2954&rft_id=info:doi/10.1098/rspb.1998.0277&rft_dat=%3Cjstor_pubme%3E50995%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=79694944&rft_id=info:pmid/9474798&rft_jstor_id=50995&rfr_iscdi=true |