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Taenia Solium Cysticercosis Using the EPICYST Transmission Model Peter Winskill1,3, Wendy E

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Taenia Solium Cysticercosis Using the EPICYST Transmission Model Peter Winskill1,3, Wendy E Winskill et al. Parasites & Vectors (2017) 10:73 DOI 10.1186/s13071-017-1988-9 RESEARCH Open Access Assessing the impact of intervention strategies against Taenia solium cysticercosis using the EPICYST transmission model Peter Winskill1,3, Wendy E. Harrison2,3, Michael D. French2,3,6, Matthew A. Dixon3, Bernadette Abela-Ridder4 and María-Gloria Basáñez3,5* Abstract Background: The pork tapeworm, Taenia solium, and associated human infections, taeniasis, cysticercosis and neurocysticercosis, are serious public health problems, especially in developing countries. The World Health Organization (WHO) has set goals for having a validated strategy for control and elimination of T. solium taeniasis/ cysticercosis by 2015 and interventions scaled-up in selected countries by 2020. Timely achievement of these internationally-endorsed targets requires that the relative benefits and effectiveness of potential interventions be explored rigorously within a quantitative framework. Methods: A deterministic, compartmental transmission model (EPICYST) was developed to capture the dynamics of the taeniasis/cysticercosis disease system in the human and pig hosts. Cysticercosis prevalence in humans, an outcome of high epidemiological and clinical importance, was explicitly modelled. A next generation matrix approach was used to derive an expression for the basic reproduction number, R0. A full sensitivity analysis was performed using a methodology based on Latin-hypercube sampling partial rank correlation coefficient index. Results: EPICYST outputs indicate that chemotherapeutic intervention targeted at humans or pigs would be highly effective at reducing taeniasis and cysticercosis prevalence when applied singly, with annual chemotherapy of humans and pigs resulting, respectively, in 94 and 74% of human cysticercosis cases averted. Improved sanitation, meat inspection and animal husbandry are less effective but are still able to reduce prevalence singly or in combination. The value of R0 for taeniasis was estimated at 1.4 (95% Credible Interval: 0.5–3.6). Conclusions: Human- and pig-targeted drug-focussed interventions appear to be the most efficacious approach from the options currently available. The model presented is a forward step towards developing an informed control and elimination strategy for cysticercosis. Together with its validation against field data, EPICYST will be a valuable tool to help reach the WHO goals and to conduct economic evaluations of interventions in varying epidemiological settings. Keywords: Cysticercosis, Neurocysticercosis, Taeniasis, Taenia solium, Tapeworm, Intervention, Mathematical modelling, EPICYST, Latin-hypercube sampling, Partial rank correlation coefficient index, Basic reproduction number * Correspondence: [email protected] 3Department of Infectious Disease Epidemiology, School of Public Health, Faculty of Medicine, Imperial College London, St Mary’s Campus, London W2 1PG, UK 5London Centre for Neglected Tropical Disease Research, Department of Infectious Disease Epidemiology, School of Public Health, Faculty of Medicine, Imperial College London, St Mary’s Campus, London W2 1PG, UK Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Winskill et al. Parasites & Vectors (2017) 10:73 Page 2 of 14 Background the field [15]. However, treatment using oxfendazole The persistence of infections by the pork tapeworm, can lead to necrotic lesions causing issues when con- Taenia solium, and the associated conditions of cysticer- suming or selling treated pork that harboured a heavy cosis and neurocysticercosis remain a major public health cyst burden [16]. concern, especially in impoverished communities that are Anthelmintic treatment of humans is an attractive op- highly dependent on pig farming [1]. The roadmap set out tion. Indeed, human treatment, with praziquantel or by the World Health Organization (WHO) in 2012 to niclosamide, has been proposed and trialled with some overcome the impact of 17 prioritised neglected tropical success [17–21]. However, to date, there has not been diseases (NTDs) called for a validated strategy, by 2015, wide scale roll out of easily accessible, affordable and re- for the control and elimination of T. solium taeniasis and liable diagnostic tests to discriminate between taeniasis cysticercosis. This roadmap also called for the implemen- and cysticercosis infection. Diagnostics are important tation of scaled-up interventions with the aim of control because treatment with praziquantel can be a potential and elimination in selected countries by 2020 [2]. Neuro- cause of severe adverse effects (SAEs) as the drug is cysticercosis remains one of the foremost causes of epi- cysticidal and can cause inflammation around dying lepsy in developing countries [3]; a recent systematic cysts in those with cysticercosis. Praziquantel therapy at review estimated that 29.0% [95% confidence intervals high doses in people harbouring a large number of oc- (95% CI): 22.9–35.5%] of people with epilepsy were also cult cysticerci may lead to severe neurological outcomes afflicted with neurocysticercosis [4]. [22]. This raises some concerns for schistosomiasis con- The multi-host life-cycle of T. solium and complica- trol programmes that deliver praziquantel at large scale tions associated with humans becoming accidental dead- in areas where the co-endemicity with T. solium is un- end hosts - resulting in the development of cysticercosis known. The impact of praziquantel on a community co- and, in some cases, the potentially fatal neurocysticerco- endemic for schistosomiasis and T. solium is the subject sis - lead to complex transmission dynamics. The vari- of an ongoing study in Malawi. The concerns about ous stages of the life-cycle, through the pig and human praziquantel-induced SAEs, combined with high logis- hosts, as well as the interface between parasite eggs and tical costs have led the focus of human preventative the environment provide a wide range of possible targets chemotherapy (PCT) away from mass drug administra- for control interventions. Whilst a variety of potential tion (MDA) [16], a strategy otherwise endorsed by the interventions have shown promise in their ability to con- WHO for the control of human helminthiases. trol taeniasis and cysticercosis, there remains a number A number of behavioural, educational and infrastruc- of challenges that must be overcome to facilitate the tural interventions target a variety of points throughout control and elimination of taeniasis and cysticercosis as the life-cycle of the parasite. Meat inspection, to screen public health problems and help the WHO to achieve its out infected pork, is one option, although a lack of sen- 2020 goals [5]. These include further development of sitivity in visual examination, poorly implemented prac- new drugs and accessible diagnostics in humans, tice and avoidance of such schemes by farmers and pig conducting randomised clinical field trials to assess pig- traders have been problematic in past efforts [23]. focussed strategies such as drug treatment and vacci- Changes to pig-husbandry practices such as indoor- nation, implementing a progression of behaviour-change rearing or corralling, aimed at limiting the contact interventions, and building transmission models to as- between pigs and the infectious agent (eggs) in the en- sess intervention strategies [6]. vironment, have been proposed but have proven hard to Current intervention strategies targeted at the pig- implement in resource-limited settings [24]. A field trial stage of the life-cycle include chemotherapeutic of a health-education intervention in Tanzania has demon- treatment and vaccination. The development and field- strated how difficult it is to instigate large impacts on testing of vaccines that protect pigs from porcine cysti- taeniasis or cysticercosis infection levels through be- cercosis are promising. A number of potential vaccines havioural change [25]. Public education interventions have has been developed, with the S3Pvac [7, 8] and TSOL18 been shown to be efficacious although their sustainabil- [9, 10] vaccines being the most encouraging, field evalu- ity has not been ascertained [25]. Improved sanitation ated, candidates. A small field trial of the TSOL18 vac- infrastructure may be effective but is reliant, in part, on cine in Cameroon demonstrated that the vaccine could economic factors out of the control of a specific inter- be highly effective in the field [11]. A second option to vention effort. target the infection in the intermediate host is anthel- Mathematical modelling of the transmission dynamics mintic chemotherapy of pigs. The most likely candidate of T. solium has the potential to be a powerful tool with for this intervention strategy is oxfendazole, which has which the problem of control and elimination of taenia- performed well at controlling the parasite in pigs sis and cysticercosis can be interrogated.
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