Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations

doi:10.3390/tropicalmed4020093

. 2019 Jun 14;4(2):93.

doi: 10.3390/tropicalmed4020093.

Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations

Eugene Ruberanziza¹, Kei Owada^{2

3}, Nicholas J Clark^{4

5}, Irenee Umulisa⁶, Giuseppina Ortu⁷, Warren Lancaster⁸, Tharcisse Munyaneza⁹, Aimable Mbituyumuremyi¹⁰, Ursin Bayisenge¹¹, Alan Fenwick¹², Ricardo J Soares Magalhães^{13

14}

Affiliations

¹ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. ruberanzizaeugene@gmail.com.
² UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. k.owada@uq.edu.au.
³ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. k.owada@uq.edu.au.
⁴ UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. nicholas.j.clark1214@gmail.com.
⁵ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. nicholas.j.clark1214@gmail.com.
⁶ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. umulisa5@gmail.com.
⁷ Schistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial College, London SW7 2AZ, UK. giuseppina_ortu@outlook.com.
⁸ The END Fund, New York, NY 10016, USA. wlancaster@end.org.
⁹ Microbiology Unit, National Reference Laboratory (NRL) Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. rukabutha@yahoo.com.
¹⁰ Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. aimable.mbituyumuremyi@rbc.gov.rw.
¹¹ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. bayursin@gmail.com.
¹² Schistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial College, London SW7 2AZ, UK. a.fenwick@imperial.ac.uk.
¹³ UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. r.magalhaes@uq.edu.au.
¹⁴ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. r.magalhaes@uq.edu.au.

PMID: 31207897
PMCID: PMC6630518
DOI: 10.3390/tropicalmed4020093

Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations

Eugene Ruberanziza et al. Trop Med Infect Dis. 2019.

. 2019 Jun 14;4(2):93.

doi: 10.3390/tropicalmed4020093.

Authors

Affiliations

¹ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. ruberanzizaeugene@gmail.com.
² UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. k.owada@uq.edu.au.
³ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. k.owada@uq.edu.au.
⁴ UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. nicholas.j.clark1214@gmail.com.
⁵ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. nicholas.j.clark1214@gmail.com.
⁶ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. umulisa5@gmail.com.
⁷ Schistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial College, London SW7 2AZ, UK. giuseppina_ortu@outlook.com.
⁸ The END Fund, New York, NY 10016, USA. wlancaster@end.org.
⁹ Microbiology Unit, National Reference Laboratory (NRL) Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. rukabutha@yahoo.com.
¹⁰ Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. aimable.mbituyumuremyi@rbc.gov.rw.
¹¹ Neglected Tropical Diseases and Other Parasitic Diseases Unit, Malaria and Other Parasitic Diseases Division, Rwanda Biomedical Center, Ministry of Health, Kigali, Rwanda. bayursin@gmail.com.
¹² Schistosomiasis Control Initiative (SCI), Department of Infectious Diseases Epidemiology, Imperial College, London SW7 2AZ, UK. a.fenwick@imperial.ac.uk.
¹³ UQ Spatial Epidemiology Laboratory, School of Veterinary Science, the University of Queensland, Gatton 4343, Queensland, Australia. r.magalhaes@uq.edu.au.
¹⁴ Children Health and Environment Program, Child Health Research Centre, The University of Queensland, South Brisbane 4101, Queensland, Australia. r.magalhaes@uq.edu.au.

PMID: 31207897
PMCID: PMC6630518
DOI: 10.3390/tropicalmed4020093

Abstract

Soil-transmitted helminth (STH) infections are globally distributed intestinal parasite infections caused by Ascaris lumbricoides, Trichuris trichiura, and hookworms (Ancylostoma duodenale and Necator americanus). STH infection constitutes a major public health threat, with heavy burdens observed in many of the world's tropical and subtropical regions. Mass drug administration and sanitation improvements can drastically reduce STH prevalence and associated morbidity. However, identifying targeted areas in need of treatment is hampered by a lack of knowledge on geographical and population-level risk factors. In this study, we applied Bayesian geostatistical modelling to data from a national school-based STH infection survey in Rwanda to (1) identify ecological and population-level risk factors and (2) provide comprehensive precision maps of infection burdens. Our results indicated that STH infections were heterogeneously distributed across the country and showed signatures of spatial clustering, though the magnitude of clustering varied among parasites. The highest rates of endemic clustering were attributed to A. lumbricoides infection. Concordant infection patterns among the three parasite groups highlighted populations currently most at-risk of morbidity. Population-dense areas in the Western and North-Western regions of Rwanda represent areas that have continued to exhibit high STH burden across two surveys and are likely in need of targeted interventions. Our maps support the need for an updated evaluation of STH endemicity in western Rwanda to evaluate progress in MDA efforts and identify communities that need further local interventions to further reduce morbidity caused by STH infections.

Keywords: Ascaris lumbricoides; Rwanda; Trichuris trichiura; hookworm; soil-transmitted helminth; spatial epidemiology.

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Conflict of interest statement

The END Fund supported STH remapping through SCI at Imperial College London and provided a research grant to the University of Queensland for additional data analysis and reporting. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Figures

**Figure 1**
Observed prevalence of *A. lumbricoides* (**Panel A**), *T. trichiura* (**Panel B**), and hookworm (**Panel C**) based on Kato-Katz in Rwanda in 2014. This figure was produced in ArcMap 10.4 (ESRI, Redlands, CA) using a shapefile representing Rwanda’s current administrative units (obtained from the data warehouse DIVA GIS).

**Figure 2**
Predicted prevalence of *A. lumbricoides* (**Panel A**), *T. trichiura* (**Panel B**), and hookworm (**Panel C**) for boys aged 12–14 years in Rwanda in 2018. Total population raster map is based on population density grid estimated using National Institute of Statistics Rwanda, Fourth Population and Housing Census 2012 data. This figure was produced in ArcMap 10.4 (ESRI, Redlands, CA) using a shapefile representing Rwanda’s current administrative units (obtained from the data warehouse DIVA GIS).

**Figure 3**
Distribution of number of children with predicted to harbour *A. lumbricoides* infection (**Panel A**), *T. trichiura* infection (**Panel B**), and hookworm (**Panel C**), (people per square kilometre) in Rwanda in 2018. Total population raster map is based on population density grid estimated using National Institute of Statistics Rwanda, Fourth Population and Housing Census 2012 data. This figure was produced in ArcMap 10.4 (ESRI, Redlands, CA) using a shapefile representing Rwanda’s current administrative units (obtained from the data warehouse DIVA GIS).

**Figure 4**
Chloropleth maps of estimated soil-transmitted (STH) helminth endemicity, represented as proportions of surveyed individuals found to be infected with at least one STH parasite (*A. lumbricoides*, *T. trichiura*, and hookworm), in Rwanda across two survey periods. This figure was produced in ArcMap 10.4 (ESRI, Redlands, CA) using a shapefile representing Rwanda’s current administrative units (obtained from the data warehouse DIVA GIS).

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References

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[1] Ortu G., Assoum M., Wittmann U., Knowles S., Clements M., Ndayishimiye O., Basáñez M.-G., Lau C., Clements A., Fenwick A., et al. The Impact of an 8-Year Mass Drug Administration Programme on Prevalence, Intensity and Co-Infections of Soil-Transmitted Helminthiases in Burundi. Parasites Vectors. 2016;9:513. doi: 10.1186/s13071-016-1794-9. - DOI - PMC - PubMed

[2] Ortu G., Assoum M., Wittmann U., Knowles S., Clements M., Ndayishimiye O., Basáñez M.-G., Lau C., Clements A., Fenwick A., et al. The Impact of an 8-Year Mass Drug Administration Programme on Prevalence, Intensity and Co-Infections of Soil-Transmitted Helminthiases in Burundi. Parasites Vectors. 2016;9:513. doi: 10.1186/s13071-016-1794-9. - DOI - PMC - PubMed

[3] De Silva N.R., Brooker S., Hotez P.J., Montresor A., Engels D., Savioli L. Soil-Transmitted Helminth Infections: Updating the Global Picture. Trends Parasitol. 2003;19:547–551. doi: 10.1016/j.pt.2003.10.002. - DOI - PubMed

[4] De Silva N.R., Brooker S., Hotez P.J., Montresor A., Engels D., Savioli L. Soil-Transmitted Helminth Infections: Updating the Global Picture. Trends Parasitol. 2003;19:547–551. doi: 10.1016/j.pt.2003.10.002. - DOI - PubMed

[5] Stoll N.R. This Wormy World. J. Parasitol. 1947;33:1–18. doi: 10.2307/3285767. - DOI - PubMed

[6] Stoll N.R. This Wormy World. J. Parasitol. 1947;33:1–18. doi: 10.2307/3285767. - DOI - PubMed

[7] Soares Magalhães R.J., Biritwum N.-K., Gyapong J.O., Brooker S., Zhang Y., Blair L., Fenwick A., Clements A.C.A. Mapping Helminth Co-Infection and Co-Intensity: Geostatistical Prediction in Ghana. PLoS Negl. Trop. Dis. 2011;5:e1200. doi: 10.1371/journal.pntd.0001200. - DOI - PMC - PubMed

[8] Soares Magalhães R.J., Biritwum N.-K., Gyapong J.O., Brooker S., Zhang Y., Blair L., Fenwick A., Clements A.C.A. Mapping Helminth Co-Infection and Co-Intensity: Geostatistical Prediction in Ghana. PLoS Negl. Trop. Dis. 2011;5:e1200. doi: 10.1371/journal.pntd.0001200. - DOI - PMC - PubMed

[9] Kightlinger L.K., Seed J.R., Kightlinger M.B. The Epidemiology of Ascaris lumbricoides, Trichuris trichiura, and Hookworm in Children in the Ranomafana Rainforest, Madagascar. J. Parasitol. 1995;81:159–169. doi: 10.2307/3283914. - DOI - PubMed

[10] Kightlinger L.K., Seed J.R., Kightlinger M.B. The Epidemiology of Ascaris lumbricoides, Trichuris trichiura, and Hookworm in Children in the Ranomafana Rainforest, Madagascar. J. Parasitol. 1995;81:159–169. doi: 10.2307/3283914. - DOI - PubMed

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Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations

Affiliations

Mapping Soil-Transmitted Helminth Parasite Infection in Rwanda: Estimating Endemicity and Identifying At-Risk Populations

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

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References

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