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.

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.

Improved methods to capture the total societal benefits of zoonotic disease control: Demonstrating the cost-effectiveness of an integrated control programme for Taenia solium, soil transmitted helminths and classical swine fever in northern Lao PDR.

BACKGROUND: Control and elimination of zoonotic diseases requires robust information about their effect on both human and livestock health in order to enable policy formulation and the allocation of resources. This study aimed to evaluate the cost-effectiveness of controlling Taenia solium taeniasis/cysticercosis in both humans and pigs, and soil-transmitted helminths (STH) in humans by integrating their control to on-going human and animal health control programmes in northern Lao People's Democratic Republic. METHOD: A cross-sectional study was carried out in 49 households, focusing on the prevalence of T. solium taenias/cysticercosis and soil transmitted helminths before and after a twelve month intervention. The village data was collected using a semi-structured questionnaire through a door-to-door survey. The village data was then projected to the wider northern Lao PDR population using stochastic modelling and cost-effectiveness ratio (after aggregating the net cost to capture both human and animal health parameters) and GDP per capita as a threshold, to determine the cost-effectiveness of the integrated control of T. solium taeniasis/ cysticercosis and STH, assuming linear scaling out of the intervention. The zoonotic DALY (zDALY) approach was also used as an alternative method of estimating the cost-effectiveness ratio of controlling T. solium taeniasis/cysticercosis in humans and pigs. FINDINGS: Using cost-effectiveness analysis after aggregating the net cost and control of T. solium taeniasis/cysticercosis alone as the base case, the study found that simultaneous control of T. solium taeniasis/cysticercosis in humans and pigs, STH in humans and Classical Swine Fever (CSF) in pigs was USD 14 per DALY averted and USD 234 per zDALY averted using zDALY method hence considered highly cost-effective whereas controlling T. solium taeniasis/cysticercosis without incorporating STH and CSF was the least cost-effective (USD 3,672 per DALY averted). Additionally, the cost-effectiveness of controlling T. solium taeniasis/cysticercosis in people and pigs using zDALY as an alternative method was USD 3,662 per zDALY averted which was quite close to our findings using the aggregate net cost method. CONCLUSION: The study showed that control of T. solium taeniasis/cysticercosis alone in humans and pigs is not cost-effective in northern Lao PDR whereas control of STH is. Consequently, integrating T. solium taeniasis/cysticercosis control with other cost-effective programmes such as STH and CSF markedly improved the cost-effectiveness of the intervention. This is especially important in low resource countries where control of zoonotic neglected tropical diseases could be integrated with the human and animal health sectors to optimize use of the limited resources. TRIAL REGISTRATION: Australia New Zealand Clinical Trials Registry (ANZCTR) ACTRN12614001067662.

Epidemiology and economic impact of bovine cysticercosis and taeniosis caused by Taenia saginata in northeastern Spain (Catalonia).

BACKGROUND: In Catalonia (north-eastern Spain), Taenia saginata has been described in cattle but its occurrence in humans is unclear. Moreover, whether cattle acquired the infection in Catalonia or outside Catalonia and its economic impact have not been investigated. This study aimed to estimate the prevalence and spatial distribution of bovine cysticercosis in Catalonia (2008-2015), and the burden from T. saginata upon the animal and human sectors in Catalonia (2013-2015). METHODS: Data on cattle diagnosed with cysticercosis at meat inspection were collected and analysed. Cattle movement history was used to identify the most likely place of bovine cysticercosis infection and to investigate its spatial distribution. Data on taeniosis treatment (niclosamide and praziquantel) costs and their supply in Catalonia as well as data on patients attending primary care with diagnosis of taeniosis were collected. The financial impact associated with T. saginata due to carcasses condemned and frozen, meat inspection and human taeniosis was estimated. RESULTS: During 2008-2015, between 18 and 107 cattle were found positive for cysticercosis each year (prevalence at slaughter of 0.010%). Movement history was available for 44% of the infected cattle and in 53% of them Catalonia was identified as the place where the infection was acquired with highest probability. Two significant bovine cysticercosis clusters were detected. The number of patients diagnosed with taeniosis in primary care during the period 2013-2016 was 41-63/year. The overall economic impact of T. saginata (2013-2015) amounted to 154,903 €/year (95% CI: 113,075-196,762). Meat inspection accounted for 81.9% (95% CI: 75.8-86.2%) of the costs, followed by costs due to carcass condemnation and freezing (9.4%; 95% CI: 6.9-12.8%), and taeniosis-associated costs (8.7%; 95% CI: 6.7-11.6%). Costs due to freezing and condemnation of carcasses reached 19,442 €/year (95% CI: 17,528-21,391) (509 €/lightly infected carcass and 1,140 €/heavily infected carcass). Taeniosis-associated costs were estimated at 12,848.5 €/year (237 €/patient). CONCLUSIONS: The public health risk of T. saginata in the area seems to be low. The economic impact due to T. saginata was mainly attributed to meat inspection. The cost due to carcass condemnation and freezing was limited compared to the revenue of the beef sector. Developing and implementing risk-based surveillance is needed to lower the costs of meat inspection. Considering cattle movements might be useful in the development of such a strategy.

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.

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.

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.

Development of a Taenia ovis transmission model and an assessment of control strategies.

The metacestode stage of the tapeworm, Taenia ovis, causes cystic lesions in the skeletal and cardiac muscle of sheep, which can result in the condemnation of the entire carcass. In recent years, Canadian farms have seen a marked increase in the number of condemnations due to T. ovis. Mathematical transmission models provide a useful tool for predicting parasite transmission and for evaluating the efficacy of potential control options. To date, no model has been developed exclusively for T. ovis. In the work described here, a compartmental, deterministic transmission model was developed to better understand the transmission dynamics of T. ovis on Canadian sheep farms. The model was intended to be practical, and represent the transmission of infection burdens in lambs that result in carcass condemnation, or transmission to canids. All transmission parameters were obtained from the literature or, when unavailable, expert opinion. The model incorporated each stage of the parasite lifecycle using the most probable transmission route on Canadian sheep farms; including definitive host (guard dogs), intermediate host (pastured lambs), and environment. Based on literature, the model performed as expected, and provided a reasonable estimate of parasite prevalence in lambs. In addition, modeling allowed the efficacy of potential control options to be evaluated and compared. Model simulations suggested that infection risk in market lambs could be eliminated through the regular treatment of guardian dogs every fifth week with an appropriate cestocide, or through eliminating carcass consumption by guardian dogs.

Cost-effective method of DNA extraction from taeniid eggs.

A new cost-effective method using silicon dioxide- and guanidine isothiocyanate-containing buffers, after previous alkaline lysis, was established for the DNA extraction from taeniid eggs isolated from canine faeces. The purified DNA can be used to amplify the species-specific 12S mitochondrial DNA of Echinococcus multilocularis in direct and nested polymerase chain reaction in order to differentiate between E. multilocularis and Taenia spp.

Taeniasis-cysticercosis in Southern Ecuador: assessment of infection status using multiple laboratory diagnostic tools.

Taenia solium-taeniasis and cysticercosis were studied in the human and porcine populations of a rural community in the Southern Ecuadorian Andes. From the 1059 inhabitants, 800 serum samples and 958 stool samples could be collected. In addition, 646 from the estimated 1148 pigs were tongue inspected. Circulating antigen was detected by enzyme linked immunosorbent assay (Ag-ELISA) in 2.25% of the human population, whereas intestinal taeniasis was detected in 1.46% by the formalin-ether technique. Following treatment and recovery of tapeworm fragments these were all identified as T. solium. Porcine cysticercosis was diagnosed in 3.56% of the pigs by tongue inspection. In addition, enzyme linked immunoelectrotransfer blot (EITB) was performed on a subset group of 100 humans to confirm the results of the Ag-ELISA. One hundred serum samples from pigs were also analysed by EITB. It appeared that 43 and 74% of humans and pigs had antibodies against T. solium cysticerci, respectively. It is concluded that contrary to the high exposure of the human population to T. solium that is suggested by EITB, the number of active cysticercosis cases, diagnosed by Ag-ELISA, was low, which may indicate endemic stability. The further use of complementary diagnostic methods for a better understanding of the epidemiology of T. solium is suggested.

Taeniasis-cysticercosis in Southern Ecuador: assessment of infection status using multiple laboratory diagnostic tools

Taenia solium-taeniasis and cysticercosis were studied in the human and porcine populations of a rural community in the Southern Ecuadorian Andes. From the 1059 inhabitants, 800 serum samples and 958 stool samples could be collected. In addition, 646 from the estimated 1148 pigs were tongue inspected. Circulating antigen was detected by enzyme linked immunosorbent assay (Ag-ELISA) in 2.25 percent of the human population, whereas intestinal taeniasis was detected in 1.46 percent by the formalin-ether technique. Following treatment and recovery of tapeworm fragments these were all identified as T. solium. Porcine cysticercosis was diagnosed in 3.56 percent of the pigs by tongue inspection. In addition, enzyme linked immunoelectrotransfer blot (EITB) was performed on a subset group of 100 humans to confirm the results of the Ag-ELISA. One hundred serum samples from pigs were also analysed by EITB. It appeared that 43 and 74 percent of humans and pigs had antibodies against T. solium cysticerci, respectively. It is concluded that contrary to the high exposure of the human population to T. solium that is suggested by EITB, the number of active cysticercosis cases, diagnosed by Ag-ELISA, was low, which may indicate endemic stability. The further use of complementary diagnostic methods for a better understanding of the epidemiology of T. solium is suggested.

Cestode vaccines: origins, current status and future prospects.

Recombinant vaccines have been developed which are highly effective in preventing infection with Taenia ovis in sheep, Taenia saginata in cattle, Taenia solium in pigs and Echinococcus granulosus in livestock animals. T. ovis and T. saginata are economically significant parasites and the commercial success or otherwise of vaccines against them will rely on their economic value. E. granulosus and T. solium are zoonotic parasites that cause cystic hydatid disease and neurocysticercosis, respectively, in humans. Vaccines against these parasites have been developed to assist with the control of transmission of the human diseases rather than for prevention of infections in livestock per se. Regions of high prevalence for cystic hydatid disease and neurocysticercosis occur primarily in the developing world. As a consequence, vaccines against them are of little or no commercially interest - they are Orphan Vaccines. Lack of commercial interest in these vaccines has made public sector support for their development necessary well beyond the research phase trough into completion of commercial scale-up and other more commercially-related assessments. Practical use of the vaccines will require commercial-scale production according to international manufacturing standards. Identifying partners and support in this endeavour is now of prime importance in efforts to achieve the potential of these vaccines as new tools for the control of cystic hydatid disease and neurocysticercosis.

Control of Taenia solium.

Control or eradication of Taenia solium cysticercosis has been achieved to date only in Europe and North America. Significant improvements in sanitary conditions and developing functional slaughterhouse control systems were primarily responsible for control in these regions. Conversely, in endemic areas of developing countries control is limited by economic and sanitary conditions: the life cycle of T. solium is sustained because pigs have access to infected faeces, and cysticercosis-infested pork is available for consumption. Interventional trials with massive human cestocidal chemotherapy, treatment of both human and porcine populations with antihelminthic drugs and/or immunotherapy and health education have shown improvements in specific settings but not yet proven to be sustainable in the long-term. In order to ensure sustainability, any given control strategy towards elimination/eradication of porcine cysticercosis should incorporate economic incentives.

Metacestodes of sheep with special reference to their epidemiological status, pathogenesis and economic implications in Fars Province, Iran.

This study was undertaken over a period of 2 years. Of 7992 sheep examined, 2088 (26.12%), 2266 (28.36%), 15 (0.19%) and 738 (9.8%) were infected with Echinococcus granulosus, Taenia hydatigena, Taenia ovis and Taenia multiceps metacestodes, respectively. The prevalence was higher in animals belonging to migratory tribal people than in those owned by the permanent residents of Fars Province. Dogs in the former group also showed significantly higher levels of infection with E. granulosus (33.3%) and Taenia spp. (40.7%) than those in the latter group. The metacestodes caused tissue damage in different organs, resulting in condemnation of meat or viscera valued at 10.2 million rials. The migration of tribal people has a direct bearing on the transmission of these parasites and must be taken into account in control planning.

[Taenia saginata: an eternal problem?]. / Taenia saginata: een eeuwig probleem?

Although the official figures of the meat inspection services show that the number of Belgian slaughtering cattle, infected with cysticercosis decreased during the last 20 years from 0.3 to 0.03%, the data collected during this study, prove that the parasite is absolutely not dying out. Detailed examination of slaughtering cattle showed that 9.5% of them are infected with cysticerci of T. saginata. This discrepancy with the official figures is due i.a. to the inappropriate detection techniques used in the slaughterhouses. Contrary to Taenia solium, T. saginata in man is far from being eradicated. Based on the number of cestocidal drugs sold in Belgium since 1980, it can be assumed that T. saginata has an average annual incidence of 0.4%. In a second chapter some epidemiological features are examined, which might explain the remarkable stability of the taeniasis-cysticercosis complex in our modern society: i.a. the high biotic potential of the parasite, the efficient dissemination of T. saginata eggs in the environment and the role of the intermediate hosts. Finally it is shown that the eradication of T. saginata is not yet feasible for the moment. A series of specific control measures are proposed in order to avoid the infection of cattle with cysticerci as well as the infection of the final host with a tapeworm.

Prevalence and economic implications of Taenia solium taeniasis and cysticercosis in Uttar Pradesh State of India.

From 1980 to 1985, 3550 pigs, 530 cattle, 370 buffalo, 1850 sheep and 2100 goat of different breeds, age and sex from different parts of Uttar Pradesh State (India) were screened for the presence of cysticerci. Economic losses due to condemnation of affected meat were calculated. The overall incidence in pigs was 9.3%. Indigenous breeds brought from rural areas had the highest infection rate (8.9%). Cysticerci were commonly observed in the muscles of fore and hind limbs, tongue, neck and brain but a few cyst were also seen in other organs including heart, kidney and spleen. No statistical difference in the rate of infection with regards to age and sex was recorded. Sheep, goat, cattle and buffalo were found negative for this infection. Also 600 human faecal samples screened for the presence of adult T. solium revealed 2% infection.