Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases

Abstract Background Schistosomiasis and infection by soil-transmitted helminths are some of the world’s most prevalent neglected tropical diseases. Infection by more than one parasite (co-infection) is common and can contribute to clinical morbidity in children. Geostatistical analyses of parasite i...

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Main Authors: Nicholas J. Clark, Kei Owada, Eugene Ruberanziza, Giuseppina Ortu, Irenee Umulisa, Ursin Bayisenge, Jean Bosco Mbonigaba, Jean Bosco Mucaca, Warren Lancaster, Alan Fenwick, Ricardo J. Soares Magalhães, Aimable Mbituyumuremyi
Format: Article
Language:English
Published: BMC 2020-03-01
Series:Parasites & Vectors
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Online Access:http://link.springer.com/article/10.1186/s13071-020-04016-2
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author Nicholas J. Clark
Kei Owada
Eugene Ruberanziza
Giuseppina Ortu
Irenee Umulisa
Ursin Bayisenge
Jean Bosco Mbonigaba
Jean Bosco Mucaca
Warren Lancaster
Alan Fenwick
Ricardo J. Soares Magalhães
Aimable Mbituyumuremyi
author_facet Nicholas J. Clark
Kei Owada
Eugene Ruberanziza
Giuseppina Ortu
Irenee Umulisa
Ursin Bayisenge
Jean Bosco Mbonigaba
Jean Bosco Mucaca
Warren Lancaster
Alan Fenwick
Ricardo J. Soares Magalhães
Aimable Mbituyumuremyi
author_sort Nicholas J. Clark
collection DOAJ
description Abstract Background Schistosomiasis and infection by soil-transmitted helminths are some of the world’s most prevalent neglected tropical diseases. Infection by more than one parasite (co-infection) is common and can contribute to clinical morbidity in children. Geostatistical analyses of parasite infection data are key for developing mass drug administration strategies, yet most methods ignore co-infections when estimating risk. Infection status for multiple parasites can act as a useful proxy for data-poor individual-level or environmental risk factors while avoiding regression dilution bias. Conditional random fields (CRF) is a multivariate graphical network method that opens new doors in parasite risk mapping by (i) predicting co-infections with high accuracy; (ii) isolating associations among parasites; and (iii) quantifying how these associations change across landscapes. Methods We built a spatial CRF to estimate infection risks for Ascaris lumbricoides, Trichuris trichiura, hookworms (Ancylostoma duodenale and Necator americanus) and Schistosoma mansoni using data from a national survey of Rwandan schoolchildren. We used an ensemble learning approach to generate spatial predictions by simulating from the CRF’s posterior distribution with a multivariate boosted regression tree that captured non-linear relationships between predictors and covariance in infection risks. This CRF ensemble was compared against single parasite gradient boosted machines to assess each model’s performance and prediction uncertainty. Results Parasite co-infections were common, with 19.57% of children infected with at least two parasites. The CRF ensemble achieved higher predictive power than single-parasite models by improving estimates of co-infection prevalence at the individual level and classifying schools into World Health Organization treatment categories with greater accuracy. The CRF uncovered important environmental and demographic predictors of parasite infection probabilities. Yet even after capturing demographic and environmental risk factors, the presences or absences of other parasites were strong predictors of individual-level infection risk. Spatial predictions delineated high-risk regions in need of anthelminthic treatment interventions, including areas with higher than expected co-infection prevalence. Conclusions Monitoring studies routinely screen for multiple parasites, yet statistical models generally ignore this multivariate data when assessing risk factors and designing treatment guidelines. Multivariate approaches can be instrumental in the global effort to reduce and eventually eliminate neglected helminth infections in developing countries.
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spelling doaj.art-4bde0d68c2b54d3e9db80c15159005dd2022-12-21T21:10:26ZengBMCParasites & Vectors1756-33052020-03-0113111610.1186/s13071-020-04016-2Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseasesNicholas J. Clark0Kei Owada1Eugene Ruberanziza2Giuseppina Ortu3Irenee Umulisa4Ursin Bayisenge5Jean Bosco Mbonigaba6Jean Bosco Mucaca7Warren Lancaster8Alan Fenwick9Ricardo J. Soares Magalhães10Aimable Mbituyumuremyi11UQ Spatial Epidemiology Laboratory, School of Veterinary Science, The University of QueenslandUQ Spatial Epidemiology Laboratory, School of Veterinary Science, The University of QueenslandNeglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical CenterSchistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial CollegeNeglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical CenterNeglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical CenterNeglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical CenterMicrobiology Unit, National Reference Laboratory (NRL) Division, Rwanda Biomedical Center, Ministry of HealthThe END FundSchistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial CollegeUQ Spatial Epidemiology Laboratory, School of Veterinary Science, The University of QueenslandMalaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of HealthAbstract Background Schistosomiasis and infection by soil-transmitted helminths are some of the world’s most prevalent neglected tropical diseases. Infection by more than one parasite (co-infection) is common and can contribute to clinical morbidity in children. Geostatistical analyses of parasite infection data are key for developing mass drug administration strategies, yet most methods ignore co-infections when estimating risk. Infection status for multiple parasites can act as a useful proxy for data-poor individual-level or environmental risk factors while avoiding regression dilution bias. Conditional random fields (CRF) is a multivariate graphical network method that opens new doors in parasite risk mapping by (i) predicting co-infections with high accuracy; (ii) isolating associations among parasites; and (iii) quantifying how these associations change across landscapes. Methods We built a spatial CRF to estimate infection risks for Ascaris lumbricoides, Trichuris trichiura, hookworms (Ancylostoma duodenale and Necator americanus) and Schistosoma mansoni using data from a national survey of Rwandan schoolchildren. We used an ensemble learning approach to generate spatial predictions by simulating from the CRF’s posterior distribution with a multivariate boosted regression tree that captured non-linear relationships between predictors and covariance in infection risks. This CRF ensemble was compared against single parasite gradient boosted machines to assess each model’s performance and prediction uncertainty. Results Parasite co-infections were common, with 19.57% of children infected with at least two parasites. The CRF ensemble achieved higher predictive power than single-parasite models by improving estimates of co-infection prevalence at the individual level and classifying schools into World Health Organization treatment categories with greater accuracy. The CRF uncovered important environmental and demographic predictors of parasite infection probabilities. Yet even after capturing demographic and environmental risk factors, the presences or absences of other parasites were strong predictors of individual-level infection risk. Spatial predictions delineated high-risk regions in need of anthelminthic treatment interventions, including areas with higher than expected co-infection prevalence. Conclusions Monitoring studies routinely screen for multiple parasites, yet statistical models generally ignore this multivariate data when assessing risk factors and designing treatment guidelines. Multivariate approaches can be instrumental in the global effort to reduce and eventually eliminate neglected helminth infections in developing countries.http://link.springer.com/article/10.1186/s13071-020-04016-2Conditional random fieldsNeglected tropical diseaseParasite co-infectionSchistosoma mansoniSoil-transmitted helminthsSpatial epidemiology
spellingShingle Nicholas J. Clark
Kei Owada
Eugene Ruberanziza
Giuseppina Ortu
Irenee Umulisa
Ursin Bayisenge
Jean Bosco Mbonigaba
Jean Bosco Mucaca
Warren Lancaster
Alan Fenwick
Ricardo J. Soares Magalhães
Aimable Mbituyumuremyi
Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
Parasites & Vectors
Conditional random fields
Neglected tropical disease
Parasite co-infection
Schistosoma mansoni
Soil-transmitted helminths
Spatial epidemiology
title Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
title_full Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
title_fullStr Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
title_full_unstemmed Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
title_short Parasite associations predict infection risk: incorporating co-infections in predictive models for neglected tropical diseases
title_sort parasite associations predict infection risk incorporating co infections in predictive models for neglected tropical diseases
topic Conditional random fields
Neglected tropical disease
Parasite co-infection
Schistosoma mansoni
Soil-transmitted helminths
Spatial epidemiology
url http://link.springer.com/article/10.1186/s13071-020-04016-2
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