Population biology of Schistosoma mating, aggregation, and transmission breakpoints: more reliable model analysis for the end-game in communities at risk
Mathematical modeling is widely used for predictive analysis of control options for infectious agents. Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that sha...
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| Veröffentlicht in: | PloS one 2014-12, Vol.9 (12), p.e115875-e115875 |
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| description | Mathematical modeling is widely used for predictive analysis of control options for infectious agents. Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that shape their reproductive success and distribution. Overdispersion and mating success are important factors to consider in modeling control options for such systems. Simpler models based on mean worm burden (MWB) formulations do not take these into account and overestimate transmission. Proposed MWB revisions have employed prescribed distributions and mating factor corrections to derive modified MWB models that have qualitatively different equilibria, including 'breakpoints' below which the parasite goes to extinction, suggesting the possibility of elimination via long-term mass-treatment control. Despite common use, no one has attempted to validate the scope and hypotheses underlying such MWB approaches. We conducted a systematic analysis of both the classical MWB and more recent "stratified worm burden" (SWB) modeling that accounts for mating and reproductive hurdles (Allee effect). Our analysis reveals some similarities, including breakpoints, between MWB and SWB, but also significant differences between the two types of model. We show the classic MWB has inherent inconsistencies, and propose SWB as a reliable alternative for projection of long-term control outcomes. |
| doi_str_mv | 10.1371/journal.pone.0115875 |
| format | Article |
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Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that shape their reproductive success and distribution. Overdispersion and mating success are important factors to consider in modeling control options for such systems. Simpler models based on mean worm burden (MWB) formulations do not take these into account and overestimate transmission. Proposed MWB revisions have employed prescribed distributions and mating factor corrections to derive modified MWB models that have qualitatively different equilibria, including 'breakpoints' below which the parasite goes to extinction, suggesting the possibility of elimination via long-term mass-treatment control. Despite common use, no one has attempted to validate the scope and hypotheses underlying such MWB approaches. We conducted a systematic analysis of both the classical MWB and more recent "stratified worm burden" (SWB) modeling that accounts for mating and reproductive hurdles (Allee effect). Our analysis reveals some similarities, including breakpoints, between MWB and SWB, but also significant differences between the two types of model. We show the classic MWB has inherent inconsistencies, and propose SWB as a reliable alternative for projection of long-term control outcomes.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0115875</identifier><identifier>PMID: 25549362</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Age ; Animal reproduction ; Animals ; Anthelmintics - therapeutic use ; Behavior, Animal ; Biology and Life Sciences ; Breakpoints ; Breeding success ; Ecology ; Females ; Formulations ; Humans ; Infections ; Mathematical analysis ; Mathematical models ; Mating ; Medicine and Health Sciences ; Models, Biological ; Parasites ; Parasitology ; Population ; Population biology ; Population Density ; Population Dynamics ; Praziquantel - therapeutic use ; Predictive control ; Reproduction ; Schistosoma ; Schistosoma - physiology ; Schistosoma mansoni ; Schistosomiasis - drug therapy ; Schistosomiasis - epidemiology ; Schistosomiasis - transmission ; Sexual Behavior, Animal ; Species extinction ; Tropical diseases</subject><ispartof>PloS one, 2014-12, Vol.9 (12), p.e115875-e115875</ispartof><rights>2014 Gurarie, King. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Gurarie, King 2014 Gurarie, King</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-aac39ace2fb18168feb1defbb6796c72dafd5388e6142504317b7c427a17cd4e3</citedby><cites>FETCH-LOGICAL-c526t-aac39ace2fb18168feb1defbb6796c72dafd5388e6142504317b7c427a17cd4e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280120/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4280120/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25549362$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Munderloh, Ulrike G.</contributor><creatorcontrib>Gurarie, David</creatorcontrib><creatorcontrib>King, Charles H</creatorcontrib><title>Population biology of Schistosoma mating, aggregation, and transmission breakpoints: more reliable model analysis for the end-game in communities at risk</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Mathematical modeling is widely used for predictive analysis of control options for infectious agents. Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that shape their reproductive success and distribution. Overdispersion and mating success are important factors to consider in modeling control options for such systems. Simpler models based on mean worm burden (MWB) formulations do not take these into account and overestimate transmission. Proposed MWB revisions have employed prescribed distributions and mating factor corrections to derive modified MWB models that have qualitatively different equilibria, including 'breakpoints' below which the parasite goes to extinction, suggesting the possibility of elimination via long-term mass-treatment control. Despite common use, no one has attempted to validate the scope and hypotheses underlying such MWB approaches. We conducted a systematic analysis of both the classical MWB and more recent "stratified worm burden" (SWB) modeling that accounts for mating and reproductive hurdles (Allee effect). Our analysis reveals some similarities, including breakpoints, between MWB and SWB, but also significant differences between the two types of model. We show the classic MWB has inherent inconsistencies, and propose SWB as a reliable alternative for projection of long-term control outcomes.</description><subject>Age</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Anthelmintics - therapeutic use</subject><subject>Behavior, Animal</subject><subject>Biology and Life Sciences</subject><subject>Breakpoints</subject><subject>Breeding success</subject><subject>Ecology</subject><subject>Females</subject><subject>Formulations</subject><subject>Humans</subject><subject>Infections</subject><subject>Mathematical analysis</subject><subject>Mathematical models</subject><subject>Mating</subject><subject>Medicine and Health Sciences</subject><subject>Models, Biological</subject><subject>Parasites</subject><subject>Parasitology</subject><subject>Population</subject><subject>Population biology</subject><subject>Population Density</subject><subject>Population Dynamics</subject><subject>Praziquantel - therapeutic use</subject><subject>Predictive control</subject><subject>Reproduction</subject><subject>Schistosoma</subject><subject>Schistosoma - physiology</subject><subject>Schistosoma mansoni</subject><subject>Schistosomiasis - drug therapy</subject><subject>Schistosomiasis - epidemiology</subject><subject>Schistosomiasis - transmission</subject><subject>Sexual Behavior, Animal</subject><subject>Species extinction</subject><subject>Tropical diseases</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNptUsuO0zAUjRCIGQp_gMASGxa0xM-kLJDQiMdII4EErK0b5yZ1x7GLnSD1U_hb3DYzmkGs_LjnnPs6RfGclivKK_p2G6bowa12weOqpFTWlXxQnNM1Z0vFSv7wzv2seJLStiwlr5V6XJwxKcWaK3Ze_PkWdpOD0QZPGhtc6PckdOS72dg0hhQGIEOO-v4Ngb6P2B-h-eFbMkbwabApHckR4XoXrB_TOzKEiCSis9A4zK8WXWaA2yebSBciGTdI0LfLHgYk1hMThmHydrSYCIwk2nT9tHjUgUv4bD4Xxc9PH39cfFleff18efHhamkkU-MSwPA1GGRdQ2uq6g4b2mLXNKpaK1OxFro2t12jooLJUnBaNZURrAJamVYgXxQvT7o7F5Kep5o0VYKWbK04zYjLE6INsNW7aAeIex3A6uNHiL2GOFrjUEsA4Dk9q1oQNeW16ZThRnBJRStFk7Xez9mmZsDWoM9TdPdE70e83eg-_NaC1SXNq1wUr2eBGH5NmEadN2DQOfAYplPdgilJD3W_-gf6_-7ECWViSClid1sMLfXBaTcsfXCanp2WaS_uNnJLurEW_wsvydYn</recordid><startdate>20141230</startdate><enddate>20141230</enddate><creator>Gurarie, David</creator><creator>King, Charles H</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141230</creationdate><title>Population biology of Schistosoma mating, aggregation, and transmission breakpoints: more reliable model analysis for the end-game in communities at risk</title><author>Gurarie, David ; King, Charles H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-aac39ace2fb18168feb1defbb6796c72dafd5388e6142504317b7c427a17cd4e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Age</topic><topic>Animal reproduction</topic><topic>Animals</topic><topic>Anthelmintics - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gurarie, David</au><au>King, Charles H</au><au>Munderloh, Ulrike G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Population biology of Schistosoma mating, aggregation, and transmission breakpoints: more reliable model analysis for the end-game in communities at risk</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-12-30</date><risdate>2014</risdate><volume>9</volume><issue>12</issue><spage>e115875</spage><epage>e115875</epage><pages>e115875-e115875</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Mathematical modeling is widely used for predictive analysis of control options for infectious agents. Challenging problems arise for modeling host-parasite systems having complex life-cycles and transmission environments. Macroparasites, like Schistosoma, inhabit highly fragmented habitats that shape their reproductive success and distribution. Overdispersion and mating success are important factors to consider in modeling control options for such systems. Simpler models based on mean worm burden (MWB) formulations do not take these into account and overestimate transmission. Proposed MWB revisions have employed prescribed distributions and mating factor corrections to derive modified MWB models that have qualitatively different equilibria, including 'breakpoints' below which the parasite goes to extinction, suggesting the possibility of elimination via long-term mass-treatment control. Despite common use, no one has attempted to validate the scope and hypotheses underlying such MWB approaches. We conducted a systematic analysis of both the classical MWB and more recent "stratified worm burden" (SWB) modeling that accounts for mating and reproductive hurdles (Allee effect). Our analysis reveals some similarities, including breakpoints, between MWB and SWB, but also significant differences between the two types of model. We show the classic MWB has inherent inconsistencies, and propose SWB as a reliable alternative for projection of long-term control outcomes.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25549362</pmid><doi>10.1371/journal.pone.0115875</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Age Animal reproduction Animals Anthelmintics - therapeutic use Behavior, Animal Biology and Life Sciences Breakpoints Breeding success Ecology Females Formulations Humans Infections Mathematical analysis Mathematical models Mating Medicine and Health Sciences Models, Biological Parasites Parasitology Population Population biology Population Density Population Dynamics Praziquantel - therapeutic use Predictive control Reproduction Schistosoma Schistosoma - physiology Schistosoma mansoni Schistosomiasis - drug therapy Schistosomiasis - epidemiology Schistosomiasis - transmission Sexual Behavior, Animal Species extinction Tropical diseases |
| title | Population biology of Schistosoma mating, aggregation, and transmission breakpoints: more reliable model analysis for the end-game in communities at risk |
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