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Inapparent infections shape the transmission heterogeneity of dengue
Abstract Transmission heterogeneity, whereby a disproportionate fraction of pathogen transmission events result from a small number of individuals or geographic locations, is an inherent property of many, if not most, infectious disease systems. For vector-borne diseases, transmission heterogeneity...
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Published in: | PNAS nexus 2023-03, Vol.2 (3), p.pgad024 |
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creator | Vazquez-Prokopec, Gonzalo M Morrison, Amy C Paz-Soldan, Valerie Stoddard, Steven T Koval, William Waller, Lance A Alex Perkins, T Lloyd, Alun L Astete, Helvio Elder, John Scott, Thomas W Kitron, Uriel |
description | Abstract
Transmission heterogeneity, whereby a disproportionate fraction of pathogen transmission events result from a small number of individuals or geographic locations, is an inherent property of many, if not most, infectious disease systems. For vector-borne diseases, transmission heterogeneity is inferred from the distribution of the number of vectors per host, which could lead to significant bias in situations where vector abundance and transmission risk at the household do not correlate, as is the case with dengue virus (DENV). We used data from a contact tracing study to quantify the distribution of DENV acute infections within human activity spaces (AS), the collection of residential locations an individual routinely visits, and quantified measures of virus transmission heterogeneity from two consecutive dengue outbreaks (DENV-4 and DENV-2) that occurred in the city of Iquitos, Peru. Negative-binomial distributions and Pareto fractions showed evidence of strong overdispersion in the number of DENV infections by AS and identified super-spreading units (SSUs): i.e. AS where most infections occurred. Approximately 8% of AS were identified as SSUs, contributing to more than 50% of DENV infections. SSU occurrence was associated more with DENV-2 infection than with DENV-4, a predominance of inapparent infections (74% of all infections), households with high Aedes aegypti mosquito abundance, and high host susceptibility to the circulating DENV serotype. Marked heterogeneity in dengue case distribution, and the role of inapparent infections in defining it, highlight major challenges faced by reactive interventions if those transmission units contributing the most to transmission are not identified, prioritized, and effectively treated. |
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Transmission heterogeneity, whereby a disproportionate fraction of pathogen transmission events result from a small number of individuals or geographic locations, is an inherent property of many, if not most, infectious disease systems. For vector-borne diseases, transmission heterogeneity is inferred from the distribution of the number of vectors per host, which could lead to significant bias in situations where vector abundance and transmission risk at the household do not correlate, as is the case with dengue virus (DENV). We used data from a contact tracing study to quantify the distribution of DENV acute infections within human activity spaces (AS), the collection of residential locations an individual routinely visits, and quantified measures of virus transmission heterogeneity from two consecutive dengue outbreaks (DENV-4 and DENV-2) that occurred in the city of Iquitos, Peru. Negative-binomial distributions and Pareto fractions showed evidence of strong overdispersion in the number of DENV infections by AS and identified super-spreading units (SSUs): i.e. AS where most infections occurred. Approximately 8% of AS were identified as SSUs, contributing to more than 50% of DENV infections. SSU occurrence was associated more with DENV-2 infection than with DENV-4, a predominance of inapparent infections (74% of all infections), households with high Aedes aegypti mosquito abundance, and high host susceptibility to the circulating DENV serotype. Marked heterogeneity in dengue case distribution, and the role of inapparent infections in defining it, highlight major challenges faced by reactive interventions if those transmission units contributing the most to transmission are not identified, prioritized, and effectively treated.</description><identifier>ISSN: 2752-6542</identifier><identifier>EISSN: 2752-6542</identifier><identifier>DOI: 10.1093/pnasnexus/pgad024</identifier><identifier>PMID: 36909820</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Biological, Health, and Medical Sciences ; Contact tracing ; Dengue ; Disease transmission ; Distribution ; Medical research ; Medicine, Experimental ; Methods</subject><ispartof>PNAS nexus, 2023-03, Vol.2 (3), p.pgad024</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences.</rights><rights>COPYRIGHT 2023 Oxford University Press</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c504t-e132ee7dcf6adcdc674b6be638f62c32c2a90cd14d6288115c182282318eeb3</citedby><cites>FETCH-LOGICAL-c504t-e132ee7dcf6adcdc674b6be638f62c32c2a90cd14d6288115c182282318eeb3</cites><orcidid>0000-0002-4035-1206 ; 0000-0003-2947-8123 ; 0000-0002-0710-270X ; 0000-0002-7518-4014 ; 0000-0001-5002-8886 ; 0000-0001-6984-7849</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10003742/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10003742/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36909820$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vazquez-Prokopec, Gonzalo M</creatorcontrib><creatorcontrib>Morrison, Amy C</creatorcontrib><creatorcontrib>Paz-Soldan, Valerie</creatorcontrib><creatorcontrib>Stoddard, Steven T</creatorcontrib><creatorcontrib>Koval, William</creatorcontrib><creatorcontrib>Waller, Lance A</creatorcontrib><creatorcontrib>Alex Perkins, T</creatorcontrib><creatorcontrib>Lloyd, Alun L</creatorcontrib><creatorcontrib>Astete, Helvio</creatorcontrib><creatorcontrib>Elder, John</creatorcontrib><creatorcontrib>Scott, Thomas W</creatorcontrib><creatorcontrib>Kitron, Uriel</creatorcontrib><title>Inapparent infections shape the transmission heterogeneity of dengue</title><title>PNAS nexus</title><addtitle>PNAS Nexus</addtitle><description>Abstract
Transmission heterogeneity, whereby a disproportionate fraction of pathogen transmission events result from a small number of individuals or geographic locations, is an inherent property of many, if not most, infectious disease systems. For vector-borne diseases, transmission heterogeneity is inferred from the distribution of the number of vectors per host, which could lead to significant bias in situations where vector abundance and transmission risk at the household do not correlate, as is the case with dengue virus (DENV). We used data from a contact tracing study to quantify the distribution of DENV acute infections within human activity spaces (AS), the collection of residential locations an individual routinely visits, and quantified measures of virus transmission heterogeneity from two consecutive dengue outbreaks (DENV-4 and DENV-2) that occurred in the city of Iquitos, Peru. Negative-binomial distributions and Pareto fractions showed evidence of strong overdispersion in the number of DENV infections by AS and identified super-spreading units (SSUs): i.e. AS where most infections occurred. Approximately 8% of AS were identified as SSUs, contributing to more than 50% of DENV infections. SSU occurrence was associated more with DENV-2 infection than with DENV-4, a predominance of inapparent infections (74% of all infections), households with high Aedes aegypti mosquito abundance, and high host susceptibility to the circulating DENV serotype. Marked heterogeneity in dengue case distribution, and the role of inapparent infections in defining it, highlight major challenges faced by reactive interventions if those transmission units contributing the most to transmission are not identified, prioritized, and effectively treated.</description><subject>Biological, Health, and Medical Sciences</subject><subject>Contact tracing</subject><subject>Dengue</subject><subject>Disease transmission</subject><subject>Distribution</subject><subject>Medical research</subject><subject>Medicine, Experimental</subject><subject>Methods</subject><issn>2752-6542</issn><issn>2752-6542</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqNkUtLxDAUhYMoKuoPcCMFNy4czatJuxIZnyC40H3IJLedSCepSSv6743MOCi4kBASbr5zuDcHoUOCzwiu2XnvdfLwPqbzvtUWU76Bdqks6USUnG7-uO-gg5ReMMZUSkJ4uY12mKhxXVG8i67uve57HcEPhfMNmMEFn4o01z0UwzzvqH1auJRyvZjDADG04MENH0VoCgu-HWEfbTW6S3CwOvfQ08318_Ru8vB4ez-9fJiYEvNhAoRRAGlNI7Q11gjJZ2IGglWNoIZRQ3WNjSXcClpVhJSGVJRWlJEKYMb20MXStR9nC7Amtxx1p_roFjp-qKCd-v3i3Vy14U2RPDuTnGaHk5VDDK8jpEHlwQx0nfYQxqSorERJOJM4o8dLtNUdqPwzIVuaL1xdSlkTIgXjmTr7g8rLwsKZ4KFxuf5LQJYCE0NKEZp1-wSrr1jVOla1ijVrjn7OvVZ8h5iB0yUQxv4ffp9xO7Ir</recordid><startdate>20230301</startdate><enddate>20230301</enddate><creator>Vazquez-Prokopec, Gonzalo M</creator><creator>Morrison, Amy C</creator><creator>Paz-Soldan, Valerie</creator><creator>Stoddard, Steven T</creator><creator>Koval, William</creator><creator>Waller, Lance A</creator><creator>Alex Perkins, T</creator><creator>Lloyd, Alun L</creator><creator>Astete, Helvio</creator><creator>Elder, John</creator><creator>Scott, Thomas W</creator><creator>Kitron, Uriel</creator><general>Oxford University Press</general><scope>TOX</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4035-1206</orcidid><orcidid>https://orcid.org/0000-0003-2947-8123</orcidid><orcidid>https://orcid.org/0000-0002-0710-270X</orcidid><orcidid>https://orcid.org/0000-0002-7518-4014</orcidid><orcidid>https://orcid.org/0000-0001-5002-8886</orcidid><orcidid>https://orcid.org/0000-0001-6984-7849</orcidid></search><sort><creationdate>20230301</creationdate><title>Inapparent infections shape the transmission heterogeneity of dengue</title><author>Vazquez-Prokopec, Gonzalo M ; Morrison, Amy C ; Paz-Soldan, Valerie ; Stoddard, Steven T ; Koval, William ; Waller, Lance A ; Alex Perkins, T ; Lloyd, Alun L ; Astete, Helvio ; Elder, John ; Scott, Thomas W ; Kitron, Uriel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c504t-e132ee7dcf6adcdc674b6be638f62c32c2a90cd14d6288115c182282318eeb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Biological, Health, and Medical Sciences</topic><topic>Contact tracing</topic><topic>Dengue</topic><topic>Disease transmission</topic><topic>Distribution</topic><topic>Medical research</topic><topic>Medicine, Experimental</topic><topic>Methods</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vazquez-Prokopec, Gonzalo M</creatorcontrib><creatorcontrib>Morrison, Amy C</creatorcontrib><creatorcontrib>Paz-Soldan, Valerie</creatorcontrib><creatorcontrib>Stoddard, Steven T</creatorcontrib><creatorcontrib>Koval, William</creatorcontrib><creatorcontrib>Waller, Lance A</creatorcontrib><creatorcontrib>Alex Perkins, T</creatorcontrib><creatorcontrib>Lloyd, Alun L</creatorcontrib><creatorcontrib>Astete, Helvio</creatorcontrib><creatorcontrib>Elder, John</creatorcontrib><creatorcontrib>Scott, Thomas W</creatorcontrib><creatorcontrib>Kitron, Uriel</creatorcontrib><collection>Oxford Open</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PNAS nexus</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vazquez-Prokopec, Gonzalo M</au><au>Morrison, Amy C</au><au>Paz-Soldan, Valerie</au><au>Stoddard, Steven T</au><au>Koval, William</au><au>Waller, Lance A</au><au>Alex Perkins, T</au><au>Lloyd, Alun L</au><au>Astete, Helvio</au><au>Elder, John</au><au>Scott, Thomas W</au><au>Kitron, Uriel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inapparent infections shape the transmission heterogeneity of dengue</atitle><jtitle>PNAS nexus</jtitle><addtitle>PNAS Nexus</addtitle><date>2023-03-01</date><risdate>2023</risdate><volume>2</volume><issue>3</issue><spage>pgad024</spage><pages>pgad024-</pages><issn>2752-6542</issn><eissn>2752-6542</eissn><abstract>Abstract
Transmission heterogeneity, whereby a disproportionate fraction of pathogen transmission events result from a small number of individuals or geographic locations, is an inherent property of many, if not most, infectious disease systems. For vector-borne diseases, transmission heterogeneity is inferred from the distribution of the number of vectors per host, which could lead to significant bias in situations where vector abundance and transmission risk at the household do not correlate, as is the case with dengue virus (DENV). We used data from a contact tracing study to quantify the distribution of DENV acute infections within human activity spaces (AS), the collection of residential locations an individual routinely visits, and quantified measures of virus transmission heterogeneity from two consecutive dengue outbreaks (DENV-4 and DENV-2) that occurred in the city of Iquitos, Peru. Negative-binomial distributions and Pareto fractions showed evidence of strong overdispersion in the number of DENV infections by AS and identified super-spreading units (SSUs): i.e. AS where most infections occurred. Approximately 8% of AS were identified as SSUs, contributing to more than 50% of DENV infections. SSU occurrence was associated more with DENV-2 infection than with DENV-4, a predominance of inapparent infections (74% of all infections), households with high Aedes aegypti mosquito abundance, and high host susceptibility to the circulating DENV serotype. Marked heterogeneity in dengue case distribution, and the role of inapparent infections in defining it, highlight major challenges faced by reactive interventions if those transmission units contributing the most to transmission are not identified, prioritized, and effectively treated.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>36909820</pmid><doi>10.1093/pnasnexus/pgad024</doi><orcidid>https://orcid.org/0000-0002-4035-1206</orcidid><orcidid>https://orcid.org/0000-0003-2947-8123</orcidid><orcidid>https://orcid.org/0000-0002-0710-270X</orcidid><orcidid>https://orcid.org/0000-0002-7518-4014</orcidid><orcidid>https://orcid.org/0000-0001-5002-8886</orcidid><orcidid>https://orcid.org/0000-0001-6984-7849</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biological, Health, and Medical Sciences Contact tracing Dengue Disease transmission Distribution Medical research Medicine, Experimental Methods |
title | Inapparent infections shape the transmission heterogeneity of dengue |
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