A qualitative assessment of the context and enabling environment for the control of Taenia solium infections in endemic settings.

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.

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.

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.

Economic implications of three strategies for the control of taeniasis.

OBJECTIVE: To evaluate the cost-effectiveness of three strategies for the control of taeniasis in a community, in terms of cost per case treated. METHODS: A study was conducted in South India to determine the prevalence of taeniasis by screening stool samples from 653 randomly chosen subjects, for coproantigens. The costs incurred in the project were used to estimate the cost per case screened and treated. A one-way sensitivity analysis was carried out for varying rates of taeniasis, different screening strategies and mass therapy. Further sensitivity analysis was carried out with different manpower and test costs. RESULTS: The rate of taeniasis as detected by ELISA for coproantigen was 3 per 1000 (2 of 653 samples). Our study showed that mass therapy without screening for taeniasis would be the most economical strategy in terms of cost per case treated if field workers are employed exclusively for either mass therapy or screening. For each strategy, costs per case treated are higher at low prevalence of taeniasis, with a sharp rise below 15%. CONCLUSIONS: In places that are endemic for taeniasis and neurocysticercosis, mass therapy or screening for taeniasis should be considered. Screening by stool microscopy is not cost-effective in terms of cost per case of taeniasis treated owing to its low sensitivity. Although the cost per case of taeniasis treated is high at low prevalence of taeniasis for all options, incorporating mass therapy into existing mass drug distribution programmes might prove to be the most cost-effective control strategy.

Methods for assessing the burden of parasitic zoonoses: echinococcosis and cysticercosis.

Cysticercosis and echinococcosis cause illness and productivity losses in human and agricultural animal populations. Recent studies suggest that these diseases have large societal impacts on endemic areas. Estimates of burden provide essential, evidence-based data for conducting cost-benefit and cost-utility analyses that will secure political will, and financial and technical resources. To evaluate the burden, the monetary and non-monetary impacts of these zoonoses on human health, agriculture and society must be considered comprehensively. In this article, we review the framework used to assess the burden of cysticercosis and echinococcosis, and the data needed to estimate the extent of the problem for societies.

Taenia solium taeniosis/cysticercosis in Asia: epidemiology, impact and issues.

Several reports of patients with cysticercosis from many countries in Asia such as India, China, Indonesia, Thailand, Korea, Taiwan and Nepal are a clear indicator of the wide prevalence of Taenia solium cysticercosis and taeniosis in these and other Asian countries. However, epidemiological data from community based studies are sparse and available only for a few countries in Asia. Cysticercosis is the cause of epilepsy in up to 50% of Indian patients presenting with partial seizures. It is also a major cause of epilepsy in Bali (Indonesia), Vietnam and possibly China and Nepal. Seroprevalence studies indicate high rates of exposure to the parasite in several countries (Vietnam, China, Korea and Bali (Indonesia)) with rates ranging from 0.02 to 12.6%. Rates of taeniosis, as determined by stool examination for ova, have also been reported to range between 0.1 and 6% in the community in India, Vietnam, China, and Bali (Indonesia). An astonishingly high rate of taeniosis of 50% was reported from an area in Nepal populated by pig rearing farmers. In addition to poor sanitation, unhealthy pig rearing practices, low hygienic standards, unusual customs such as consumption of raw pork is an additional factor contributing to the spread of the disease in some communities of Asia. Undoubtedly, cysticercosis is a major public health problem in several Asian countries effecting several million people by not only causing neurological morbidity but also imposing economic hardship on impoverished populations. However, there are wide variations in the prevalence rates in different regions and different socio-economic groups in the same country. It is important to press for the recognition of cysticercosis as one of the major public health problems in Asia that needs to be tackled vigorously by the governments and public health authorities of the region.

Annual economic loss caused by Taenia saginata asiatica taeniasis in three endemic areas of east Asia.

The Taenia saginata-like tapeworm in East Asia has been designed as a separate subspecies of T. saginata. It was named as T. saginata asiatica and the classical T. saginata as T. saginata saginata. In the course of conducting experimental infections and morphological studies, a large number of adult worms of T. saginata asiatica was collected. It is possible to estimate the annual economic loss caused by this infection, since the worm load and the weight of worm habored by each infected person were determined from the collection. In the mountainous areas of Taiwan, the infection rate of T. saginata asiatica taeniasis was 11.0%, the worm load was 1.6 worms/case, and the average weight of an adult worm was 20.5 g. The annual economic loss was estimated to be US$ 11,327,423. On Cheju Island of Korea, the infection rate was 6.0%, the worm load was 2 worms/case, and the average weight of an adult worm was 19.3 g. The annual economic loss was estimated to be US$ 13,641,021. On Samosir Island of Indonesia, the infection rate was 21%, the worm load was 1.8 worms/case, and the average weight of an adult worm was 22 g. The annual economic loss was estimated to be US$ 2,425,500. These figures indicate that taeniasis is not only a significant public health problem but also an important economic problem in East Asia.

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.

Economic losses resulting from food-borne parasitic zoonoses.

Economic losses resulting from food-borne parasitic zoonoses are difficult to assess. Estimating the global economic impact of these diseases is handicapped by inadequate information on the prevalence and public health importance of parasitic zoonoses for most countries. However, the economic losses caused by certain zoonoses has been estimated for some regions and in these instances the costs are significant. In Mexico, for example, porcine cysticercosis is responsible for a loss of more than one-half of the national investment in swine production and for more than US$17 million annually in hospitalization and treatment costs for humans with neurocysticercosis. For all of Latin America, porcine cysticercosis accounts for an economic loss of US$164 million. In Africa, losses of one to two billion dollars per year due to bovine cysticercosis have been reported. Human toxoplasmosis in the United States is estimated to be an annual economic/public health burden of more than US$400 million. The implication from these examples and other are discussed. A set of recommendations is presented for obtaining the necessary information needed to permit assigning to food-borne parasitic zoonoses their appropriate priority within each country's complex economic and public health problems.

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.