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 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 R2 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.

[1]  J. Utzinger,et al.  Effect of preventive chemotherapy with praziquantel on schistosomiasis among school-aged children in sub-Saharan Africa: a spatiotemporal modelling study , 2021, The Lancet. Infectious diseases.

[2]  Vitus Tankpa,et al.  Climate Change, Flood Disaster Risk and Food Security Nexus in Northern Ghana , 2021, Frontiers in Sustainable Food Systems.

[3]  J. Utzinger,et al.  Urogenital schistosomiasis infection prevalence targets to determine elimination as a public health problem based on microhematuria prevalence in school-age children , 2021, PLoS neglected tropical diseases.

[4]  G. Kang,et al.  Prediction of hookworm prevalence in southern India using environmental parameters derived from Landsat 8 remotely sensed data. , 2019, International journal for parasitology.

[5]  A. Montresor,et al.  Sustained preventive chemotherapy for soil-transmitted helminthiases leads to reduction in prevalence and anthelminthic tablets required , 2019, Infectious Diseases of Poverty.

[6]  S. Sloan,et al.  Deforestation is driven by agricultural expansion in Ghana's forest reserves , 2019, Scientific African.

[7]  E. Naumova,et al.  The use of remotely sensed environmental parameters for spatial and temporal schistosomiasis prediction across climate zones in Ghana , 2019, Environmental Monitoring and Assessment.

[8]  J. Utzinger,et al.  Improving spatial prediction of Schistosoma haematobium prevalence in southern Ghana through new remote sensors and local water access profiles , 2018, PLoS neglected tropical diseases.

[9]  Zhi Huang,et al.  Application of random forest, generalised linear model and their hybrid methods with geostatistical techniques to count data: Predicting sponge species richness , 2017, Environ. Model. Softw..

[10]  T. Esch,et al.  Breaking new ground in mapping human settlements from space – The Global Urban Footprint , 2017, 1706.04862.

[11]  I. Bogoch,et al.  Assessment of global guidelines for preventive chemotherapy against schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. , 2016, The Lancet. Infectious diseases.

[12]  Benjamin F. Leutner,et al.  Use of an ecologically relevant modelling approach to improve remote sensing-based schistosomiasis risk profiling. , 2015, Geospatial health.

[13]  Mirko S. Winkler,et al.  Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. , 2015, The Lancet. Infectious diseases.

[14]  S. Liang,et al.  Surveillance systems for neglected tropical diseases: global lessons from China’s evolving schistosomiasis reporting systems, 1949–2014 , 2014, Emerging Themes in Epidemiology.

[15]  C. King,et al.  Human schistosomiasis , 2014, The Lancet.

[16]  nasa,et al.  LANDSAT data users handbook , 2013 .

[17]  Alan Fenwick,et al.  Mapping Helminth Co-Infection and Co-Intensity: Geostatistical Prediction in Ghana , 2011, PLoS neglected tropical diseases.

[18]  Ralf Wieland,et al.  Classification in conservation biology: A comparison of five machine-learning methods , 2010, Ecol. Informatics.

[19]  G. Standing The international labour organisation , 2010 .

[20]  Simon Brooker,et al.  Spatial heterogeneity of parasite co-infection: Determinants and geostatistical prediction at regional scales , 2009, International journal for parasitology.

[21]  S. Brooker,et al.  Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm , 2006, The Lancet.

[22]  R. Tibshirani,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction , 2004 .

[23]  S. Brooker,et al.  Soil-transmitted helminth infections: updating the global picture. , 2003, Trends in parasitology.

[24]  Eric R. Ziegel,et al.  The Elements of Statistical Learning , 2003, Technometrics.

[25]  D. Altman,et al.  Applying the right statistics: analyses of measurement studies , 2003, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[26]  A. N. Strahler Quantitative analysis of watershed geomorphology , 1957 .

[27]  Mirko S. Winkler,et al.  Spatial and temporal distribution of soil-transmitted helminth infection in sub-Saharan Africa: a systematic review and geostatistical meta-analysis. , 2015, The Lancet. Infectious diseases.

[28]  Y. Walz Remote sensing for disease risk profiling: a spatial analysis of schistosomiasis in West Africa , 2014 .

[29]  U. Grömping Dependence of Variable Importance in Random Forests on the Shape of the Regressor Space , 2009 .

[30]  Schistosomiasis Richtlijn Schistosomiasis Richtlijn , 2006 .

[31]  S. Brooker,et al.  The potential of geographical information systems and remote sensing in the epidemiology and control of human helminth infections. , 2000, Advances in parasitology.

[32]  H. Sabbaghian,et al.  Host-parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. 3. Effect of water temperature on the ability of miracidia to infect snails. , 1966, Bulletin of the World Health Organization.