Clinical characteristics and management of neurocysticercosis patients: a retrospective assessment of case reports from Europe.

OBJECTIVES: Neurocysticercosis (NCC) is a parasitic disease caused by the larval stage of the tapeworm Taenia solium. NCC mainly occurs in Africa, Latin America and South-East Asia and can cause a variety of clinical signs/symptoms. Although it is a rare disease in Europe, it should nonetheless be considered as a differential diagnosis. The aim of this study was to describe clinical characteristics and management of patients with NCC diagnosed and treated in Europe. METHODS: We conducted a systematic search of published and unpublished data on patients diagnosed with NCC in Europe (2000-2019) and extracted demographic, clinical and radiological information on each case, if available. RESULTS: Out of 293 identified NCC cases, 59% of patients presented initially with epileptic seizures (21% focal onset); 52% presented with headache and 54% had other neurological signs/symptoms. The majority of patients had a travel or migration history (76%), mostly from/to Latin America (38%), Africa (32%) or Asia (30%). Treatment varied largely depending on cyst location and number. The outcome was favorable in 90% of the cases. CONCLUSIONS: Management of NCC in Europe varied considerably but often had a good outcome. Travel and migration to and from areas endemic for T. solium will likely result in continued low prevalence of NCC in Europe. Therefore, training and guidance of clinicians is recommended for optimal patient management.

Assessment of Hygienic Practices in Beef Cattle Slaughterhouses and Retail Shops in Bishoftu, Ethiopia: Implications for Public Health.

Understanding the potential drivers of microbial meat contamination along the entire meat supply chain is needed to identify targets for interventions to reduce the number of meatborne bacterial outbreaks. We assessed the hygienic practices in cattle slaughterhouses (28 employees) and retail shops (127 employees) through face-to-face interviews and direct personal observations. At the slaughterhouses, stunning, de-hiding and evisceration in vertical position, carcass washing and separate storage of offal were the identified good practices. Lack of hot water baths, absence of a chilling room, infrequent hand washing, insufficiently trained staff and irregular medical check-up were practices that lead to unhygienic handling of carcasses. At the retail shops, cleaning equipment using soap and hot water (81%), storing unsold meat in refrigerators (92%), concrete floors and white painted walls and ceilings were good practices. Adjacently displaying offal and meat (39%), lack of a cold chain, wrapping meat with plastic bags and newspapers, using a plastic or wooden cutting board (57%), infrequent washing of equipment and floors, and inadequately trained employees were practices that could result in unhygienic handling of beef. Our study identified unhygienic practices both at the slaughterhouses and retail shops that can predispose the public to meatborne infections, which could be improved through training and implementation of quality control systems.

Strategies for tackling Taenia solium taeniosis/cysticercosis: A systematic review and comparison of transmission models, including an assessment of the wider Taeniidae family transmission models.

BACKGROUND: The cestode Taenia solium causes the neglected (zoonotic) tropical disease cysticercosis, a leading cause of preventable epilepsy in endemic low and middle-income countries. Transmission models can inform current scaling-up of control efforts by helping to identify, validate and optimise control and elimination strategies as proposed by the World Health Organization (WHO). METHODOLOGY/PRINCIPAL FINDINGS: A systematic literature search was conducted using the PRISMA approach to identify and compare existing T. solium transmission models, and related Taeniidae infection transmission models. In total, 28 modelling papers were identified, of which four modelled T. solium exclusively. Different modelling approaches for T. solium included deterministic, Reed-Frost, individual-based, decision-tree, and conceptual frameworks. Simulated interventions across models agreed on the importance of coverage for impactful effectiveness to be achieved. Other Taeniidae infection transmission models comprised force-of-infection (FoI), population-based (mainly Echinococcus granulosus) and individual-based (mainly E. multilocularis) modelling approaches. Spatial structure has also been incorporated (E. multilocularis and Taenia ovis) in recognition of spatial aggregation of parasite eggs in the environment and movement of wild animal host populations. CONCLUSIONS/SIGNIFICANCE: Gaps identified from examining the wider Taeniidae family models highlighted the potential role of FoI modelling to inform model parameterisation, as well as the need for spatial modelling and suitable structuring of interventions as key areas for future T. solium model development. We conclude that working with field partners to address data gaps and conducting cross-model validation with baseline and longitudinal data will be critical to building consensus-led and epidemiological setting-appropriate intervention strategies to help fulfil the WHO targets.

Stepwise approach for the control and eventual elimination of Taenia solium as a public health problem.

BACKGROUND: Taenia solium taeniosis/cysticercosis is a public health and agricultural problem, especially in low-income countries, and has been ranked the top foodborne parasitic hazard globally. In 2012, the World Health Organization published a roadmap that called for a validated strategy for T. solium control and elimination by 2015. This goal has not been met, and validated evidence of effective control or elimination in endemic countries is still incomplete. Measuring and evaluating success of control programmes remains difficult, as locally acceptable targets have not been defined as part of the 2012 roadmap nor from other sources, and the performance of tools to measure effect are limited. DISCUSSION: We believe that an international agreement supported by the tripartite World Health Organization, Food and Agriculture Organization of the United Nations, and World Organisation for Animal Health is needed to facilitate endemic countries in publicising SMART (Specific, Measurable, Achievable/attainable, Relevant, Time-bound) country-level control target goals. These goals should be achievable through locally acceptable adoption of options from within a standardised 'intervention tool-kit', and progress towards these goals should be monitored using standardised and consistent diagnostics. Several intervention tools are available which can contribute to control of T. solium, but the combination of these - the most effective control algorithm - still needs to be identified. In order to mount control efforts and ensure political commitment, stakeholder engagement and funding, we argue that a stepwise approach, as developed for Rabies control, is necessary if control efforts are to be successful and sustainable. CONCLUSIONS: The stepwise approach can provide the framework for the development of realistic control goals of endemic areas, the implementation of intervention algorithms, and the standardised monitoring of the evaluation of the progress towards obtaining the control target goals and eventually elimination.

A quantitative risk assessment for human Taenia solium exposure from home slaughtered pigs in European countries.

BACKGROUND: Taenia solium, a zoonotic tapeworm, is responsible for about a third of all preventable epilepsy human cases in endemic regions. In Europe, adequate biosecurity of pig housing and meat inspection practices have decreased the incidence of T. solium taeniosis and cysticercosis. Pigs slaughtered at home may have been raised in suboptimal biosecurity conditions and slaughtered without meat inspection. As a result, consumption of undercooked pork from home slaughtered pigs could pose a risk for exposure to T. solium. The aim of this study was to quantify the risk of human T. solium exposure from meat of home slaughtered pigs, in comparison to controlled slaughtered pigs, in European countries. A quantitative microbial risk assessment model (QMRA) was developed and porcine cysticercosis prevalence data, the percentage of home slaughtered pigs, meat inspection sensitivity, the cyst distribution in pork and pork consumption in five European countries, Bulgaria, Germany, Poland, Romania and Spain, were included as variables in the model. This was combined with literature about cooking habits to estimate the number of infected pork portions eaten per year in a country. RESULTS: The results of the model showed a 13.83 times higher prevalence of contaminated pork portions from home slaughtered pigs than controlled slaughtered pigs. This difference is brought about by the higher prevalence of cysticercosis in pigs that are home raised and slaughtered. Meat inspection did not affect the higher exposure from pork that is home slaughtered. Cooking meat effectively lowered the risk of exposure to T. solium-infected pork. CONCLUSIONS: This QMRA showed that there is still a risk of obtaining an infection with T. solium due to consumption of pork, especially when pigs are reared and slaughtered at home, using data of five European countries that reported porcine cysticercosis cases. We propose systematic reporting of cysticercosis cases in slaughterhouses, and in addition molecularly confirming suspected cases to gain more insight into the presence of T. solium in pigs and the risk for humans in Europe. When more data become available, this QMRA model could be used to evaluate human exposure to T. solium in Europe and beyond.

Bovine cysticercosis and taeniosis: The effect of an alternative post-mortem detection method on prevalence and economic impact.

In Europe, bovine cysticercosis (BCC) is detected by routine meat inspection (MI) at the slaughterhouse. The prevalence of BCC in Belgium based on MI is estimated at 0.23%. MI has a known low sensitivity for animals with localised infections and alternative detection techniques should be considered. A mathematical scenario-analysis model was built to determine the current prevalence of BCC in Belgium based on MI results combined with results of dissection of the predilection sites (PS) and the B158/B60 Ag-ELISA on serum of 614 carcasses found negative on MI. Additionally, the impact of the introduction of the B158/B60 Ag-ELISA at slaughter on the prevalence of BCC and taeniosis and on the economic impact related to Taenia saginata was estimated for Belgium. Data for estimating the economic impact were gathered from multiple sources within the meat and human health sectors and included value loss for infected carcasses, inspection costs, carcass destruction costs, cattle insurance costs and costs related to taeniosis (consultation physician, drugs and laboratory test). The model estimated the current prevalence of BCC to be 42.5% (95% CI: 32.4-60.7%) and the sensitivity of the MI for viable and degenerated cysticerci at only 0.54% (95% CI: 0.37-0.71%). A total of 213,344 viable cysticerci (95% CI: 122,962-386.249) were estimated to be present in the infected carcasses in one year and only 408 (95% CI: 356-464) of these were present in the carcasses detected at current MI. The annual number of human taeniosis cases is estimated at 11,000 by using the sale numbers of niclosamide in Belgium. Implementation of the Ag-ELISA at slaughter (Se = 36.37%; Sp = 99.36%) would greatly reduce the prevalence of BCC to 0.6% and the number of taeniosis cases to 89 in year 10. Unfortunately, the accompanying resulting increase in costs for the animal owners, slaughterhouses and the insurance company, would be extremely high in the first years. Cattle owners would suffer losses of up to €21 million in the first year after implementation of the Ag-ELISA (compared to an annual loss of €3.5 million in the current situation), slaughterhouses of €10 million (compared to €200,000 currently) and the insurance company of almost €6 million (compared to €2.3 million profit currently). Therefore, implementation of the Ag-ELISA might not be feasible and other options for controlling T. saginata should be investigated.

Economic impact of bovine cysticercosis and taeniosis caused by Taenia saginata in Belgium.

BACKGROUND: Bovine cysticercosis (BCC) (due to Taenia saginata) is often claimed to cause considerable economic losses to the livestock industry, particularly in beef cattle, but recent studies estimating the economic impact are lacking. The current study aimed to quantify the annual economic impact of BCC in Belgium from 2012 to 2016, by gathering data from diverse sources in the meat and human health sectors. RESULTS: In Belgium, on average, 15 carcasses with generalised infections and 1168 carcasses with localised ones are detected upon meat inspection each year. The highest proportion of the total economic losses due to bovine cysticercosis were borne by the cattle owners with an average economic cost of €3,408,455/year: €2,954,061/year due to BCC insurance, €453,024/year due to value losses of beef of uninsured carcasses (i.e. freezing process) and €1370/year due to destruction costs of uninsured carcasses with generalised infections. The slaughterhouses suffered an economic impact of €210,806/year. They were responsible for inspection costs related to meat inspection in general, administration, processing and deboning of infected carcasses (€597,856/year), value losses (€34,848/year) and destruction costs (€105/year) of carcasses insured by the slaughterhouses (unofficial insurance) (5% of slaughtered animals). On the other hand, the slaughterhouses gained a total of €422,004/year due to unofficial insurance fees. Thirty percent of all slaughtered animals were officially insured against BCC and the insurance company generated an income of €2,322,337/year. The economic impact related to taeniosis (10,991 patients annually) amounted to a maximum of €795,858/year. CONCLUSION: BCC and taeniosis due to T. saginata have a large economic impact in Belgium, mainly due to the insurance costs for BCC. These results indicate the need for reducing the number of BCC and taeniosis cases to avoid the costs and losses related to this parasite.

Taenia solium from a community perspective: Preliminary costing data in the Katete and Sinda districts in Eastern Zambia.

The tapeworm Taenia solium is endemic in Zambia, however its socioeconomic cost is unknown. During a large-scale interventional study conducted in Zambia, baseline economic costs of human and porcine T. solium infections were measured. Questionnaire surveys were conducted within three neighbourhoods in Zambia's Eastern province in 2015 and 2016. A human health questionnaire, capturing costs of clinical symptoms commonly attributable to human cysticercosis and taeniasis, was conducted in randomly selected households (n = 267). All pig-keeping households were administered a pig socioeconomic questionnaire (n = 271) that captured pig demographic data, costs of pig-keeping, and economic losses from porcine cysticercosis. Of all respondents 62% had reportedly experienced at least one of the surveyed symptoms. Seizure-like episodes were reported by 12%, severe chronic headaches by 36%, and vision problems by 23% of respondents. These complaints resulted in 147 health care consultations and 17 hospitalizations in the five years preceding the study, and an estimated productivity loss of 608 working days per year. Of all pigs 69% were bought within villages. Nearly all adult pigs were sold to local traders, and tongue palpation for detection of cysticerci was commonly performed. Reportedly, 95% of pig owners could not sell tongue-positive pigs, while infected pigs fetched only 45% of the normal sale value. These preliminary costing data indicate that human and porcine T. solium infections substantially impact endemic areas of Eastern Zambia. A full socioeconomic burden assessment may enable improved T. solium management in sub-Saharan Africa.

Preliminary assessment of the computer-based Taenia solium educational program 'The Vicious Worm' on knowledge uptake in primary school students in rural areas in eastern Zambia.

OBJECTIVE: The zoonotic helminth Taenia solium is endemic in Zambia, causing human (taeniasis and (neuro)cysticercosis) and pig (porcine cysticercosis) diseases with high health, social and economic burdens. We aimed to evaluate the impact of a health educational program intended to lead to powerful and cumulative improvements in knowledge, attitudes and practices that decrease parasite transmission and disease occurrence. METHODS: Half-day health education workshops were conducted in three primary schools in the highly endemic Eastern Province of Zambia, using the computer-based T. solium educational program 'The Vicious Worm'. Questionnaires were administered before and after the educational component to determine the program's impact on knowledge uptake in primary school students. RESULTS: In total, 99 students participated: 38 males and 61 females, with a median age of 14 years (range 10-18 years). Baseline general knowledge of T. solium, including awareness of the different human and pig disease states, and disease diagnosis, treatment and prevention, was quite high (average score 62%) and consistent across all three study areas. Participants' knowledge had significantly increased after the educational component, particularly regarding parasite transmission and disease prevention. CONCLUSION: Preliminary assessment of 'The Vicious Worm' indicates it is an effective tool for the short-term T. solium education of primary school students in Zambia. Follow-up studies are planned to assess the longer term impact of the program on knowledge uptake in the study neighbourhoods. Inclusion of tailored 'The Vicious Worm' educational workshops should be considered in integrated cysticercosis control programs in endemic areas of sub-Saharan Africa.

Assessment of the repeatability and border-plate effects of the B158/B60 enzyme-linked-immunosorbent assay for the detection of circulating antigens (Ag-ELISA) of Taenia saginata.

The monoclonal antibody-based circulating antigen detecting ELISA (B158/B60 Ag-ELISA) has been used elaborately in several studies for the diagnosis of human, bovine and porcine cysticercosis. Interpretation of test results requires a good knowledge of the test characteristics, including the repeatability and the effect of the borders of the ELISA plates. Repeatability was tested for 4 antigen-negative and 5 antigen-positive reference bovine serum samples by calculating the Percentage Coefficient of Variation (%CV) within and between plates, within and between runs, overall, for two batches of monoclonal antibodies and by 2 laboratory technicians. All CV values obtained were below 20% (except one: 24.45%), which indicates a good repeatability and a negligible technician error. The value of 24.45% for indicating the variability between batches of monoclonal antibodies for one positive sample is still acceptable for repeatability measures. Border effects were determined by calculating the %CV values between the inner and outer wells of one plate for 2 positive serum samples. Variability is a little more present in the outer wells but this effect is very small and no significant border effect was found.

Correction: The Influence of Socio-economic, Behavioural and Environmental Factors on Taenia spp. Transmission in Western Kenya: Evidence from a Cross-Sectional Survey in Humans and Pigs.

[This corrects the article DOI: 10.1371/journal.pntd.0004223.].

The Influence of Socio-economic, Behavioural and Environmental Factors on Taenia spp. Transmission in Western Kenya: Evidence from a Cross-Sectional Survey in Humans and Pigs.

UNLABELLED: Taenia spp. infections, particularly cysticercosis, cause considerable health impacts in endemic countries. Despite previous evidence of spatial clustering in cysticercosis and the role of environmental factors (e.g. temperature and humidity) in the survival of eggs, little research has explored these aspects of Taenia spp. EPIDEMIOLOGY: In addition, there are significant gaps in our understanding of risk factors for infection in humans and pigs. This study aimed to assess the influence of socio-economic, behavioural and environmental variables on human and porcine cysticercosis. A cross-sectional survey for human taeniasis (T. solium and T. saginata), human cysticercosis (T. solium) and pig cysticercosis (T. solium) in 416 households in western Kenya was carried out. These data were linked to questionnaire responses and environmental datasets. Multi-level regression was used to examine the relationships between covariates and human and porcine cysticercosis. The HP10 Ag-ELISA sero-prevalence (suggestive of cysticercosis) was 6.6% for humans (95% CI 5.6%-7.7%), and 17.2% for pigs (95% CI 10.2%-26.4%). Human taeniasis prevalence, based on direct microscopic observation of Taenia spp. eggs (i.e. via microscopy results only) was 0.2% (95% CI 0.05%-0.5%). Presence of Taenia spp. antigen in both humans and pigs was significantly associated with a range of factors, including positive correlations with land cover. The presence of HP10 antigen in humans was correlated (non-linearly) with the proportion of land within a 1 km buffer that was flooding agricultural land and grassland (odds ratio [OR] = 1.09 and 0.998; p = 0.03 and 0.03 for the linear and quadratic terms respectively), gender (OR = 0.58 for males compared to females, p = 0.02), level of education (OR = 0.62 for primary level education versus no formal education, p = 0.09), use of well water for drinking (OR = 2.76 for those who use well water versus those who do not, p = 0.02) and precipitation (OR = 0.998, p = 0.02). Presence of Taenia spp. antigen in pigs was significantly correlated with gender and breeding status of the pig (OR = 10.35 for breeding sows compared to boars, p = 0.01), and the proportion of land within a 1 km buffer that was flooding agricultural land and grassland (OR = 1.04, p = 0.004). These results highlight the role of multiple socio-economic, behavioural and environmental factors in Taenia spp. transmission patterns. Environmental contamination with Taenia spp. eggs is a key issue, with landscape factors influencing presence of Taenia spp. antigens in both pigs and humans.

Distribution and Potential Indicators of Hospitalized Cases of Neurocysticercosis and Epilepsy in Ecuador from 1996 to 2008.

BACKGROUND: Epilepsy is one of the most common signs of Neurocysticercosis (NCC). In this study, spatial and temporal variations in the incidence of hospitalized cases (IHC) of epilepsy and NCC in Ecuadorian municipalities were analyzed. Additionally, potential socio-economic and landscape indicators were evaluated in order to understand in part the macro-epidemiology of the Taenia solium taeniasis/cysticercosis complex. METHODOLOGY: Data on the number of hospitalized epilepsy and NCC cases by municipality of residence were obtained from morbidity-hospital systems in Ecuador. SatScan software was used to determine whether variations in the IHC of epilepsy and NCC in space and time. In addition, several socio-economic and landscape variables at municipality level were used to study factors intervening in the macro-epidemiology of these diseases. Negative Binomial regression models through stepwise selection and Bayesian Model Averaging (BMA) were used to explain the variations in the IHC of epilepsy and NCC. PRINCIPAL FINDINGS: Different clusters were identified through space and time. Traditional endemic zones for NCC and epilepsy, recognized in other studies were confirmed in our study. However, for both disorders more recent clusters were identified. Among municipalities, an increasing tendency for IHC of epilepsy, and a decreasing tendency for the IHC of NCC were observed over time. In contrast, within municipalities a positive linear relationship between both disorders was found. An increase in the implementation of systems for eliminating excrements would help to reduce the IHC of epilepsy by 1.00% (IC95%; 0.2%-1.8%) and by 5.12% (IC95%; 3.63%-6.59%) for the IHC of NCC. The presence of pig production was related to IHC of NCC. CONCLUSION/SIGNIFICANCE: Both disorders were related to the lack of an efficient system for eliminating excrements. Given the appearance of recent epilepsy clusters, these locations should be studied in depth to discriminate epilepsies due to NCC from epilepsies due to other causes. Field studies are needed to evaluate the true prevalence of cysticercosis in humans and pigs in different zones of the country in order to better implement and manage prevention and/or control campaigns.