Nicholas Ngwili

Background: 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. Methods: 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. Results: 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. Conclusions: 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.

Taenia solium taeniasis/cysticercosis in humans and pigs remains endemic to Uganda. Although, looking at the lifecycle of the parasite, the risk factors are well known, and many biomedical control options exist – no substantial progress has been made in the eradication of T. solium infections in Uganda to date. Contextual factors including socioeconomic, cultural and infrastructural factors, may influence the adoption of interventions. A community-based study using mixed methods and relying on system effects modelling approach was carried out between March and April 2021 in Kamuli district, Eastern Uganda, and Hoima district, Western Uganda. System effects modelling is a non-linear methodology that captures the varied nature of the unique, individually lived experiences and aggregates them to reflect what is experienced at a population level. The aim of the study was to capture individual stakeholder perceptions on the consequences of T. solium infections and barriers to practice known control options. Overall, 27 factors were identified by 192 participants as consequences of being infected with neurocysticercosis (NCC). For taeniasis, 35 factors were identified with 700 edges/connections made by the participants. Enlargement of stomach, weight loss, diarrhoea, weakness, and stunted growth were the most important consequences. Although porcine cysticercosis (PCC) seemed to be poorly understood by the participants, 14 factors were identified which included poor pig growth, loss of market for pig/pork, and poor pork quality. The study also identified important barriers hindering the adoption of control practices, including lack of knowledge on transmission, sociocultural factors, and resource constraints. For women, lack of knowledge on the mode of transmission and lack of a toilet in the compound ranked highly as important barriers with a weighted degree of 31 and 21, respectively, meaning they were identified by more participants unlike men who ranked lack of a toilet first with a weighted degree of 39, followed by lack of knowledge at 24. Different barriers are associated with the adoption of T. solium control practices among community members, stakeholders, and farmers. Despite efforts to address T. solium infections, misconceptions and limited understanding persist among stakeholders, particularly regarding NCC and its associated consequences. The system effects approach supports developing contextualized interventions to help in the control of the diseases associated with this parasite.

Taenia (T.) solium is a zoonotic parasite causing three diseases: Taeniasis and cysticercosis in humans and porcine cysticercosis in pigs. Although biomedically, the transmission of the parasite can be easily interrupted at six points along the life cycle, the contextual factors that may influence the adoption of these control strategies in Uganda remain unclear. This study assessed the stakeholders' knowledge, attitudes, and perceptions relating to the six control strategies for T. solium infections in Kamuli and Hoima districts, Uganda. A total of 22 focus group discussions (FGD) were conducted with pig farmers, community leaders, pig/pork traders, animal health assistants, and human health assistants. In addition, nine key informant interviews were held with senior officials in the ministries of agriculture and health and other relevant agencies at the district level. The results showed differential, limited, and fragmented knowledge on T. solium infections among stakeholders. Pig farmers, community leaders, and pig/pork traders had almost no knowledge and were often confused regarding the differences existing between T. solium and other gastro-intestinal infections in pigs and humans. Pig confinement, pit latrine construction, coverage, maintenance, and sustained use are influenced by cultural, socio-economic, and physical/ environmental factors of the study population and area. Proper sensitisation programmes and health education interventions should target all, but with appropriately focused material to suit the different stakeholder categories. Reminders or nudges may be needed to ensure that increase in knowledge translates to changes in practise. Intervention programmes should also aim to overcome challenges created by the various contextual factors operating in the specific endemic areas.

A study was carried out in Kamuli and Hoima districts in Eastern and Western regions of Uganda to determine the Taenia solium porcine cysticercosis (PCC) and gastrointestinal (GI) parasites co-infection status in pigs. One hundred sixty-one households were selected randomly and visited between November and December 2019. A household questionnaire was administered, and faecal and blood samples were collected from at least one pig older than 3 months per household. A blood sample was obtained from a jugular venipuncture, and a rectal faecal sample was obtained. Taenia spp. circulating antigen levels in the sample sera were tested using a commercial enzyme-linked immunosorbent assay kit, apDia™ cysticercosis Ag ELISA. The modified McMaster technique was used to identify and quantify the GI parasites. The apparent animal-level seroprevalence for PCC was 4.8% (95% CI 2.7–7.1) and differed across the two districts (p = 0.018). At the pig herd level, the prevalence was 9.7% (95% CI 5.5–14.4). The prevalence of the different nematode eggs and coccidian oocysts in the two districts was as follows: strongyles 79.0% (95% CI 74.3–83.6), coccidia 73.3% (95% CI 68.3–78.6), Trichuris spp. 7.4% (95% CI 4.9–10.6), Strongyloides ransomi 2.1 (95% CI 0.7–3.5) and Ascaris spp. 4.9 (95% CI 2.8–7.4). Overall, across the two districts, the arithmetic mean for the oocysts per gram (OPG) for coccidia was 2042.2 ± 5776.1, and eggs per gram (EPG) were the highest in strongyles 616.1 ± 991. Overall, 57.4% of the porcine cysticercosis seropositive pigs were also positive for at least one of the gastrointestinal helminths which included strongyles, Strongyloides ransomi, Trichuris spp. and Ascaris spp. The co-infection status of pigs with both PCC and GI parasites demonstrated by this study can provide an incentive for integrating the control and management of both parasites with oxfendazole. Further studies are required to understand the feasibility of using oxfendazole including cost–benefit analysis and the acceptability by local stakeholders for the control of T. solium cysticercosis and gastrointestinal parasites in pigs.

Background: Taenia solium (T. solium), is a zoonotic helminth causing three diseases namely; taeniasis (in humans), neurocysticercosis (NCC, in humans) and porcine cysticercosis (PCC, in pigs) and is one of the major foodborne diseases by burden. The success or failure of control options against this parasite in terms of reduced prevalence or incidence of the diseases may be attributed to the contextual factors which underpin the design, implementation, and evaluation of control programmes. Methodology/Principal findings: The study used a mixed method approach combining systematic literature review (SLR) and key informant interviews (KII). The SLR focused on studies which implemented T. solium control programmes and was used to identify the contextual factors and enabling environment relevant to successful inception, planning and implementation of the interventions. The SLR used a protocol pre-registered at the International prospective register of systematic reviews (PROSPERO) number CRD42019138107 and followed PRISMA guidelines on reporting of SLR. To further highlight the importance and interlinkage of these contextual factors, KII were conducted with researchers/implementers of the studies included in the SLR. The SLR identified 41 publications that had considerations of the contextual factors. They were grouped into efficacy (10), effectiveness (28) and scale up or implementation (3) research studies. The identified contextual factors included epidemiological, socioeconomic, cultural, geographical and environmental, service and organizational, historical and financial factors. The enabling environment was mainly defined by policy and strategies supporting T. solium control. Conclusion/Significance: Failure to consider the contextual factors operating in target study sites was shown to later present challenges in project implementation and evaluation that negatively affected expected outcomes. This study highlights the importance of fully considering the various domains of the context and integrating these explicitly into the plan for implementation and evaluation of control programmes. Explicit reporting of these aspects in the resultant publication is also important to guide future work. The contextual factors highlighted in this study may be useful to guide future research and scale up of disease control programmes and demonstrates the importance of close multi-sectoral collaboration in a One Health approach.