{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T08:16:18Z","timestamp":1772180178075,"version":"3.50.1"},"reference-count":50,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T00:00:00Z","timestamp":1661126400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"The Netherlands Initiative for Capacity development in Higher Education (NICHE)","award":["NICHE\/RWA\/07"],"award-info":[{"award-number":["NICHE\/RWA\/07"]}]},{"name":"University of Twente, The Netherlands","award":["NICHE\/RWA\/07"],"award-info":[{"award-number":["NICHE\/RWA\/07"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["TropicalMed"],"abstract":"<jats:p>Background. Soil-transmitted helminths (STH) are parasitic diseases with significant public health impact. Analysis is generally based on cross-sectional prevalence surveys; outcomes are mostly aggregated to larger spatial units. However, recent research demonstrates that infection levels and spatial patterns differ between STH species and tend to be localized. Methods. Incidence data of STHs including roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura) and hookworms per primary health facility for 2008 were linked to spatially delineated primary health center service areas. Prevalence data per district for individual and combined STH infections from the 2008 nationwide survey in Rwanda were also obtained. Results. A comparison of reported prevalence and incidence data indicated significant positive correlations for roundworm (R2 = 0.63) and hookworm (R2 = 0.27). Weak positive correlations were observed for whipworm (R2 = 0.02) and the three STHs combined (R2 = 0.10). Incidence of roundworm and whipworm were found to be focalized with significant spatial autocorrelation (Moran\u2019s I &gt; 0: 0.05\u20130.38 and p \u2264 0.03), with (very) high incidence rates in some focal areas. In contrast, hookworm incidence is ubiquitous and randomly distributed (Moran\u2019s I &gt; 0: 0.006 and p = 0.74) with very low incidence rates. Furthermore, an exploratory regression analysis identified relationships between helminth infection cases and potential environmental and socio-economic risk factors. Conclusions. Findings show that the spatial distribution of STH incidence is significantly associated with soil properties (sand proportion and pH), rainfall, wetlands and their uses, population density and proportion of rural residents. Identified spatial patterns are important for guiding STH prevention and control programs.<\/jats:p>","DOI":"10.3390\/tropicalmed7080202","type":"journal-article","created":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T23:49:56Z","timestamp":1661212196000},"page":"202","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Using Routinely Collected Health Records to Identify the Fine-Resolution Spatial Patterns of Soil-Transmitted Helminth Infections in Rwanda"],"prefix":"10.3390","volume":"7","author":[{"given":"Elias","family":"Nyandwi","sequence":"first","affiliation":[{"name":"Centre for Geographic Information Systems and Remote Sensing, College of Science and Technology, University of Rwanda, KN 73 Street, (Avenue de l\u2019Arm\u00e9e), Kigali P.O. Box 4285, Rwanda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9970-5902","authenticated-orcid":false,"given":"Tom","family":"Veldkamp","sequence":"additional","affiliation":[{"name":"Faculty of Geo-Information Science and Earth Observation, University of Twente, 7522 NB Enschede, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sherif","family":"Amer","sequence":"additional","affiliation":[{"name":"Faculty of Geo-Information Science and Earth Observation, University of Twente, 7522 NB Enschede, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eugene","family":"Ruberanziza","sequence":"additional","affiliation":[{"name":"Rwanda Biomedical Centre, Malaria and Other Parasitic Diseases Unit, KG 644 Street, Kimihurura, Kigali P.O. Box 4285, Rwanda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nadine","family":"Rujeni","sequence":"additional","affiliation":[{"name":"School of Health Sciences, College of Medicine and Health Sciences, University of Rwanda, KN 73 Street, (Avenue de l\u2019Arm\u00e9e), Kigali P.O. Box 4285, Rwanda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Irene\u00e9","family":"Umulisa","sequence":"additional","affiliation":[{"name":"Rwanda Biomedical Centre, Malaria and Other Parasitic Diseases Unit, KG 644 Street, Kimihurura, Kigali P.O. Box 4285, Rwanda"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/1756-3305-6-359","article-title":"Bayesian geostatistical modelling of soil-transmitted helminth survey data in the People\u2019s Republic of China","volume":"6","author":"Lai","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_2","unstructured":"TRAC+ (2008). National Prevalence Survey on Soil-Transmitted Helminths and Schistosomiasis in School-Aged Children, TRAC PLUS-Centre for Infectious Disease Control. Access Project."},{"key":"ref_3","unstructured":"WHO (2010). Rwanda-Country Profile. Preventive Chemotherapy and Transmission Control, WHO: Department of Control of Neglected Tropical Diseases."},{"key":"ref_4","first-page":"397","article-title":"A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni","volume":"14","author":"Katz","year":"1972","journal-title":"Rev. Inst. Med. Trop. Sao Paulo"},{"key":"ref_5","first-page":"812","article-title":"Removing the neglect from neglected tropical diseases: The Rwandan experience 2008\u20132010","volume":"7","author":"Ruxin","year":"2012","journal-title":"Glob. Public Health Int. J. Res. Policy Pract."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/s40249-016-0212-z","article-title":"Schistosomiasis and soil-transmitted helminthiasis in Rwanda: An update on their epidemiology and control","volume":"6","author":"Rujeni","year":"2017","journal-title":"Infect. Dis. Poverty"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Ruberanziza, E., Owada, K., Clark, N.J., Umulisa, I., Ortu, G., Lancaster, W., Munyaneza, T., Mbituyumuremyi, A., Bayisenge, U., and Fenwick, A. (2019). Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations. Trop. Med. Infect. Dis., 4.","DOI":"10.3390\/tropicalmed4020093"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1186\/s13071-020-04016-2","article-title":"Parasite associations predict infection risk: Incorporating co-infections in predictive models for neglected tropical diseases","volume":"13","author":"Clark","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/S1995-7645(14)60088-2","article-title":"Prevalence of gastrointestinal helminthic infections and associated risk factors among schoolchildren in Tilili town, northwest Ethiopia","volume":"7","author":"Abera","year":"2014","journal-title":"Asian Pac. J. Trop. Med."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Pullan, R.L., Kabatereine, N.B., Quinnell, R.J., and Brooker, S. (2010). Spatial and Genetic Epidemiology of Hookworm in a Rural Community in Uganda. PLoS Negl. Trop. Dis., 4.","DOI":"10.1371\/journal.pntd.0000713"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1111\/tmi.12205","article-title":"Prevalence and clustering of soil-transmitted helminth infections in a tribal area in southern India","volume":"18","author":"Kaliappan","year":"2013","journal-title":"Trop. Med. Int. Health"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1111\/j.1365-3156.2009.02440.x","article-title":"Spatial co-distribution of neglected tropical diseases in the East African Great Lakes region: Revisiting the justification for integrated control","volume":"15","author":"Clements","year":"2010","journal-title":"Trop. Med. Int. Health"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Halpenny, C.M., Paller, C., Koski, K.G., Vald\u00e9s, V.E., and Scott, M.E. (2013). Regional, Household and Individual Factors that Influence Soil Transmitted Helminth Reinfection Dynamics in Preschool Children from Rural Indigenous Panam\u00e1. PLoS Negl. Trop. Dis., 7.","DOI":"10.1371\/journal.pntd.0002070"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Strunz, E.C., Addiss, D.G., Stocks, M.E., Ogden, S., Utzinger, J., and Freeman, M.C. (2014). Water, Sanitation, Hygiene, and Soil-Transmitted Helminth Infection: A Systematic Review and Meta-Analysis. PLoS Med., 11.","DOI":"10.1371\/journal.pmed.1001620"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1017\/S0031182099004503","article-title":"Seasonal variation in development and survival of Ascaris suum and Trichuris suis eggs on pastures","volume":"119","author":"Larsen","year":"1999","journal-title":"Parasitology"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Nyandwi, E., Veldkamp, A., Amer, S., Karema, C., and Umulisa, I. (2017). Schistosomiasis mansoni incidence data in Rwanda can improve prevalence assessments, by providing high-resolution hotspot and risk factors identification. BMC Public Health, 17.","DOI":"10.1186\/s12889-017-4816-4"},{"key":"ref_17","unstructured":"NISR (2014). Fourth Rwanda Population and Housing Census. Thematic Report: Population Projections, NISR."},{"key":"ref_18","unstructured":"Rwanda (2012). Ministerial Instruction\/Min\/2012 Defining the Functioning Norms of Private Health Establishment in Rwanda, Kigali, Rwanda."},{"key":"ref_19","unstructured":"National Institute of Statistics of Rwanda (2011). The Third Integrated Household Living Conditions Survey, National Institute of Statistics of Rwanda."},{"key":"ref_20","unstructured":"Swedesurvey (2010). Project of Rwanda National Land Use and Development Master Plan, Report for Production of Ortho Photo in Rwanda, Swedesurvey."},{"key":"ref_21","first-page":"91","article-title":"Terrain Shape Index: Quantifying Effect of Minor Landforms on Tree Height","volume":"35","author":"McNab","year":"1989","journal-title":"For. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.agee.2005.10.006","article-title":"Environmental assessment tools for multi-scale land resources information systems: A case study of Rwanda","volume":"114","author":"Verdoodt","year":"2006","journal-title":"Agric. Ecosyst. Environ."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1965","DOI":"10.1002\/joc.1276","article-title":"Very High Resolution Interpolated Climate Surfaces for Global Land Areas","volume":"25","author":"Hijmans","year":"2005","journal-title":"Int. J. Climatol."},{"key":"ref_24","unstructured":"REMA (2008). Etablissement d\u2019un Inventaire National Rapide des Marais et \u00c9laboration de 5 Avant-Projets D\u2019arr\u00eat\u00e9s Minist\u00e9riels Relatifs Aux Marais, Rwanda Environment Management Authority Kigali."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.1007\/s10113-015-0905-z","article-title":"Regional climate sensitivity of wetland environments in Rwanda: The need for a location-specific approach","volume":"16","author":"Nyandwi","year":"2015","journal-title":"Reg. Environ. Change"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Hurlimann, E., Schur, N., Boutsika, K., Stensgaard, A., Laserna de Himpsl, M., Ziegelbauer, K., Laizer, N., Camenzind, L., Di Pasquale, A., and Ekpo, U. (2011). Toward an open-access global database for mapping, control, and surveillance of neglected tropical diseases. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0001404"},{"key":"ref_27","unstructured":"Rothman, K.J. (2012). Epidemiology: An Introduction, Oxford University Press, Inc.. [2nd ed.]."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/s10651-007-0064-6","article-title":"Accounting for rate instability and spatial patterns in the boundary analysis of cancer mortality maps","volume":"15","author":"Goovaerts","year":"2008","journal-title":"Environ. Ecol. Stat."},{"key":"ref_29","unstructured":"CDC (2014, November 05). BioMedware SpaceStat-Empirical Bayesian Smoothing. Available online: https:\/\/www.biomedware.com\/files\/documentation\/spacestat\/Statistics\/Smoothing\/Empirical_Bayesian_Smoothing.htm."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/j.1538-4632.1992.tb00261.x","article-title":"The Analysis of Spatial Association by Use of Distance Statistics","volume":"24","author":"Getis","year":"1992","journal-title":"Geogr. Anal."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1111\/j.1538-4632.2008.00727.x","article-title":"A History of the Concept of Spatial Autocorrelation: A Geographer\u2019s Perspective","volume":"40","author":"Getis","year":"2007","journal-title":"Geogr. Anal."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/j.envsoft.2007.10.004","article-title":"Automated regression-based statistical downscaling tool","volume":"23","author":"Hessami","year":"2008","journal-title":"Environ. Model. Softw."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.envres.2014.07.029","article-title":"Developing small-area predictions for smoking and obesity prevalence in the United States for use in Environmental Public Health Tracking","volume":"134","author":"Davies","year":"2014","journal-title":"Environ. Res."},{"key":"ref_34","unstructured":"Lehmann, E.L. (1998). Nonparametrics: Statistical Methods Based on Ranks, Prentice Hall. [1st ed.]."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.catena.2005.03.001","article-title":"Spatially distributed data for erosion model calibration and validation: The Ganspoel and Kinderveld datasets","volume":"61","author":"Govers","year":"2005","journal-title":"CATENA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.tca.2015.04.013","article-title":"Prediction of the enthalpies of vaporization for room-temperature ionic liquids: Correlations and a substitution-based additive scheme","volume":"609","author":"Kabo","year":"2015","journal-title":"Thermochim. Acta"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1016\/j.acra.2015.03.001","article-title":"Multimodality 3D Tumor Segmentation in HCC Patients Treated with TACE","volume":"22","author":"Wang","year":"2015","journal-title":"Acad. Radiol."},{"key":"ref_38","first-page":"274","article-title":"Review of Regression Methods in Biostatistics: Linear, Logistic, Survival, and Repeated Measures Models by Vittinghoff, Glidden, Shiboski, and McCulloch","volume":"5","author":"Lemeshow","year":"2005","journal-title":"Strata"},{"key":"ref_39","first-page":"335","article-title":"Efficacy of alebendazole and mebendazole in the treatment of Ascaris and Trichuris infections","volume":"40","author":"Legesse","year":"2002","journal-title":"Ethiop. Med. J."},{"key":"ref_40","unstructured":"Montresor, A., Crompton, D.W.T., Hall, A., Bundy, D.A.P., and Savioli, L. (1998). Guidelines for Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level, WHO."},{"key":"ref_41","unstructured":"Malesu, M.M., Oduor, A.R., Chrogony, K., Nyolei, D., Gachene, C.K.K., Biamah, E.K., O\u2019Neil, M., Ilyama, M., Mogoi, J., and Rwanda Irrigation Master Plan (2017, January 30). The Government of Rwanda, Ministry of Agriculture and Animal Resources, Ebony Company Limited and World Agroforestry Centre (ICRAF). Nairobi, Kenya. Available online: http:\/\/www.worldagroforestry.org\/downloads\/Publications\/PDFS\/B16738.pdf."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"253","DOI":"10.3855\/jidc.2539","article-title":"Epidemiology of soil-transmitted helminths, Schistosoma mansoni, and haematocrit values among schoolchildren in Ethiopia","volume":"7","author":"Abera","year":"2012","journal-title":"J. Infect. Dev. Ctries."},{"key":"ref_43","unstructured":"MINECOFIN (2015). Demographic and Health Survey [DHS] 2014\/2015 Key Findings, MINECOFIN."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/S0065-308X(05)62007-6","article-title":"Global epidemiology, ecology and control of soil-transmitted helminth infections","volume":"62","author":"Brooker","year":"2006","journal-title":"Adv. Parasitol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"175","DOI":"10.4103\/0974-777X.81696","article-title":"Prevention of Soil-transmitted Helminth Infection","volume":"3","year":"2011","journal-title":"J. Glob. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"794","DOI":"10.4269\/ajtmh.14-0039","article-title":"Dramatic Decrease in Prevalence of Soil-Transmitted Helminths and New Insights Into Intestinal Protozoa in Children Living in the Chaco Region, Bolivia","volume":"92","author":"Macchioni","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_47","unstructured":"Thaxton, M. (2009). Integrating Population, Health, and Environment in Rwanda, Population Reference Bureau."},{"key":"ref_48","unstructured":"Phillips, D.R. (1990). Health and Health Care in the Third World, Longman Scientific & Technical."},{"key":"ref_49","unstructured":"NISR, MOH, and ICF International (2012). Rwanda Demographic and Health Survey 2010, ICF International."},{"key":"ref_50","unstructured":"USAID\/Rwanda (2006). Rwanda HMIS Assessment Report, USAID. 9 May 2006."}],"container-title":["Tropical Medicine and Infectious Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2414-6366\/7\/8\/202\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:13:33Z","timestamp":1760141613000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2414-6366\/7\/8\/202"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,22]]},"references-count":50,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["tropicalmed7080202"],"URL":"https:\/\/doi.org\/10.3390\/tropicalmed7080202","relation":{},"ISSN":["2414-6366"],"issn-type":[{"value":"2414-6366","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,22]]}}}