Spatial and temporal risk mapping of human and porcine Taenia solium infections in Malawi: a systematic review and geostatistical approach

Abstract

Taenia solium, colloquially called the pork tapeworm, is a zoonotic parasite with a human definitive host and a porcine intermediate host. Humans can become an aberrant intermediate host due to accidental ingestion of parasite eggs from the environment or through autoinfection, resulting in human cysticercosis (HCC), or neurocysticercosis (NCC) if the central nervous system is infected. Pigs become infected with the larval stage, porcine cysticercosis (PCC), through the ingestion of parasite eggs shed by humans through defecation. Malawi has been classified as endemic for T. solium by the WHO based on the presence of key risk factors; however, the subnational distribution is not known. To ensure the appropriate resources are mobilized to support targeted future T. solium control measures in Malawi, there is a need to understand the variation in T. solium endemicity status across the country. The current study uses a systematic literature review (SLR) using a pre-registered protocol; (PROSPERO CRD42023411044) to collate all available evidence on T. solium in Malawi. A geospatial risk mapping approach was conducted based on data from Malawi Demographic and Health Surveys (MDHS), and pig density data from the Food and Agriculture Organization (FAO) database to create geospatial risk maps of endemic subnational areas for 2000, 2004, 2010, and 2016. To create a single composite risk factor map for the four years from the MDHS, each parameter was plotted as a binary variable with the high or low risk categories and overlaid into a single composite risk factor classification. Additional data from hospital records on NCC and meat inspection records across several Agricultural Development Divisions (ADDs) were also collected. A total of 9 studies were identified through the SLR, with 8 studies focused on HCC, including one study studying both HCC and PCC, and one study on PCC. The review of the hospital reports captured 38 reports of NCC, with the cases being from around the location of the two major hospitals. PCC rates in slaughter animals substantially varied among the six ADDs, with the highest rates being in Mzuzu ADD, with 3.7 cases per 100 ps-years-1, and in Salima ADD, with 4.5 cases 100 ps-years-1. Geospatial risk mapping results for the years 2000 to 2016 indicated that PCC risk factors exhibited substantial geographic and temporal variation. Areas at highest risk, with the presence of all three risk factors, were predominantly found in the central and southern districts of Malawi across years. High pig density and poverty in combination were evident across Malawi in 2000; however, these areas declined in northern districts between 2004 and 2016 while remaining consistent in central districts. The combined map from the four data streams did not provide validation for the risk maps but provided more robust evidence about the potential endemicity of the parasite in Malawi. Most studies identified from the SLR were case reports and mostly focused on HCC, with very limited literature available in terms of population-based studies. The confluence of high levels of poverty, poor sanitation, and high pig densities is evident in central and southern districts, indicating potential T. solium endemic areas warranting further investigation. Review of NCC cases from hospital records and PCC rates in slaughtered animals across ADDs further supports prioritizing these areas. Targeted epidemiological and socio-economic studies to inform interventions in the possibly hyperendemic areas are urgently required.