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How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana

BACKGROUND: Schistosomiasis and soil-transmitted helminth infections are among the neglected tropical diseases (NTDs) affecting primarily marginalized communities in low- and middle-income countries. Surveillance data for NTDs are typically sparse, and hence, geospatial predictive modeling based on...

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Autores principales: Kulinkina, Alexandra V., Farnham, Andrea, Biritwum, Nana-Kwadwo, Utzinger, Jürg, Walz, Yvonne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10310024/
https://www.ncbi.nlm.nih.gov/pubmed/37327211
http://dx.doi.org/10.1371/journal.pntd.0011424
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author Kulinkina, Alexandra V.
Farnham, Andrea
Biritwum, Nana-Kwadwo
Utzinger, Jürg
Walz, Yvonne
author_facet Kulinkina, Alexandra V.
Farnham, Andrea
Biritwum, Nana-Kwadwo
Utzinger, Jürg
Walz, Yvonne
author_sort Kulinkina, Alexandra V.
collection PubMed
description BACKGROUND: Schistosomiasis and soil-transmitted helminth infections are among the neglected tropical diseases (NTDs) affecting primarily marginalized communities in low- and middle-income countries. Surveillance data for NTDs are typically sparse, and hence, geospatial predictive modeling based on remotely sensed (RS) environmental data is widely used to characterize disease transmission and treatment needs. However, as large-scale preventive chemotherapy has become a widespread practice, resulting in reduced prevalence and intensity of infection, the validity and relevance of these models should be re-assessed. METHODOLOGY: We employed two nationally representative school-based prevalence surveys of Schistosoma haematobium and hookworm infections from Ghana conducted before (2008) and after (2015) the introduction of large-scale preventive chemotherapy. We derived environmental variables from fine-resolution RS data (Landsat 8) and examined a variable distance radius (1–5 km) for aggregating these variables around point-prevalence locations in a non-parametric random forest modeling approach. We used partial dependence and individual conditional expectation plots to improve interpretability of results. PRINCIPAL FINDINGS: The average school-level S. haematobium prevalence decreased from 23.8% to 3.6% and that of hookworm from 8.6% to 3.1% between 2008 and 2015. However, hotspots of high-prevalence locations persisted for both infections. The models with environmental data extracted from a buffer radius of 2–3 km around the school location where prevalence was measured had the best performance. Model performance (according to the R(2) value) was already low and declined further from approximately 0.4 in 2008 to 0.1 in 2015 for S. haematobium and from approximately 0.3 to 0.2 for hookworm. According to the 2008 models, land surface temperature (LST), modified normalized difference water index, elevation, slope, and streams variables were associated with S. haematobium prevalence. LST, slope, and improved water coverage were associated with hookworm prevalence. Associations with the environment in 2015 could not be evaluated due to low model performance. CONCLUSIONS/SIGNIFICANCE: Our study showed that in the era of preventive chemotherapy, associations between S. haematobium and hookworm infections and the environment weakened, and thus predictive power of environmental models declined. In light of these observations, it is timely to develop new cost-effective passive surveillance methods for NTDs as an alternative to costly surveys, and to focus on persisting hotspots of infection with additional interventions to reduce reinfection. We further question the broad application of RS-based modeling for environmental diseases for which large-scale pharmaceutical interventions are in place.
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spelling pubmed-103100242023-06-30 How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana Kulinkina, Alexandra V. Farnham, Andrea Biritwum, Nana-Kwadwo Utzinger, Jürg Walz, Yvonne PLoS Negl Trop Dis Research Article BACKGROUND: Schistosomiasis and soil-transmitted helminth infections are among the neglected tropical diseases (NTDs) affecting primarily marginalized communities in low- and middle-income countries. Surveillance data for NTDs are typically sparse, and hence, geospatial predictive modeling based on remotely sensed (RS) environmental data is widely used to characterize disease transmission and treatment needs. However, as large-scale preventive chemotherapy has become a widespread practice, resulting in reduced prevalence and intensity of infection, the validity and relevance of these models should be re-assessed. METHODOLOGY: We employed two nationally representative school-based prevalence surveys of Schistosoma haematobium and hookworm infections from Ghana conducted before (2008) and after (2015) the introduction of large-scale preventive chemotherapy. We derived environmental variables from fine-resolution RS data (Landsat 8) and examined a variable distance radius (1–5 km) for aggregating these variables around point-prevalence locations in a non-parametric random forest modeling approach. We used partial dependence and individual conditional expectation plots to improve interpretability of results. PRINCIPAL FINDINGS: The average school-level S. haematobium prevalence decreased from 23.8% to 3.6% and that of hookworm from 8.6% to 3.1% between 2008 and 2015. However, hotspots of high-prevalence locations persisted for both infections. The models with environmental data extracted from a buffer radius of 2–3 km around the school location where prevalence was measured had the best performance. Model performance (according to the R(2) value) was already low and declined further from approximately 0.4 in 2008 to 0.1 in 2015 for S. haematobium and from approximately 0.3 to 0.2 for hookworm. According to the 2008 models, land surface temperature (LST), modified normalized difference water index, elevation, slope, and streams variables were associated with S. haematobium prevalence. LST, slope, and improved water coverage were associated with hookworm prevalence. Associations with the environment in 2015 could not be evaluated due to low model performance. CONCLUSIONS/SIGNIFICANCE: Our study showed that in the era of preventive chemotherapy, associations between S. haematobium and hookworm infections and the environment weakened, and thus predictive power of environmental models declined. In light of these observations, it is timely to develop new cost-effective passive surveillance methods for NTDs as an alternative to costly surveys, and to focus on persisting hotspots of infection with additional interventions to reduce reinfection. We further question the broad application of RS-based modeling for environmental diseases for which large-scale pharmaceutical interventions are in place. Public Library of Science 2023-06-16 /pmc/articles/PMC10310024/ /pubmed/37327211 http://dx.doi.org/10.1371/journal.pntd.0011424 Text en © 2023 Kulinkina et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Kulinkina, Alexandra V.
Farnham, Andrea
Biritwum, Nana-Kwadwo
Utzinger, Jürg
Walz, Yvonne
How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title_full How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title_fullStr How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title_full_unstemmed How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title_short How do disease control measures impact spatial predictions of schistosomiasis and hookworm? The example of predicting school-based prevalence before and after preventive chemotherapy in Ghana
title_sort how do disease control measures impact spatial predictions of schistosomiasis and hookworm? the example of predicting school-based prevalence before and after preventive chemotherapy in ghana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10310024/
https://www.ncbi.nlm.nih.gov/pubmed/37327211
http://dx.doi.org/10.1371/journal.pntd.0011424
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