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In Vitro and in Vivo Trematode Models for Chemotherapeutic Studies

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In Vitro and in Vivo Trematode Models for Chemotherapeutic Studies 589 In vitro and in vivo trematode models for chemotherapeutic studies J. KEISER* Department of Medical Parasitology and Infection Biology, Swiss Tropical Institute, CH-4002 Basel, Switzerland (Received 27 June 2009; revised 7 August 2009 and 26 October 2009; accepted 27 October 2009; first published online 7 December 2009) SUMMARY Schistosomiasis and food-borne trematodiases are chronic parasitic diseases affecting millions of people mostly in the developing world. Additional drugs should be developed as only few drugs are available for treatment and drug resistance might emerge. In vitro and in vivo whole parasite screens represent essential components of the trematodicidal drug discovery cascade. This review describes the current state-of-the-art of in vitro and in vivo screening systems of the blood fluke Schistosoma mansoni, the liver fluke Fasciola hepatica and the intestinal fluke Echinostoma caproni. Examples of in vitro and in vivo evaluation of compounds for activity are presented. To boost the discovery pipeline for these diseases there is a need to develop validated, robust high-throughput in vitro systems with simple readouts. Key words: Schistosoma mansoni, Fasciola hepatica, Echinostoma caproni, in vitro, in vivo, drug discovery, chemotherapy. INTRODUCTION by chemotherapy. However, only two drugs are currently available: triclabendazole against fascio- Thus far approximately 6000 species in the sub-class liasis and praziquantel against the other food-borne Digenea, phylum Platyhelminthes have been de- trematode infections and schistosomiasis (Keiser and scribed in the literature. Among them, only a dozen Utzinger, 2004; Keiser et al. 2005). Hence, there is a or so species parasitize humans. These include need for discovery and development of new drugs, the blood flukes (five species of Schistosoma), liver particularly in view of growing concern about re- flukes (Clonorchis sinensis, Fasciola gigantica, Fasciola sistance developing to existing drugs. Triclabend- hepatica, Opisthorchis felineus and Opisthorchis azole resistance is already common in veterinary viverrini), lung flukes (Paragonimus spp.) and intes- parasitology (Keiser et al. 2005) and the extensive use tinal flukes (e.g. Echinostoma spp. and Fasciolopsis of praziquantel resistance in mass drug adminis- buski) (Cox, 1993; Keiser and Utzinger, 2009). These tration programs has raised concern regarding the parasites are the causative agents of a complex of selection of drug resistant schistosomes (Melmann some acute, but mainly chronic infections: schisto- et al. 2009). somiasis and food-borne trematodiases (Keiser and There has been little incentive to invest in the Utzinger, 2007; Utzinger et al. 2007; Davis, 2009; discovery and development of trematodicidal drugs. Sithiathaworn et al. 2009). It is currently estimated While public-private partnerships have been formed that 1400 million people are at risk of schistosomiasis for some of the neglected tropical diseases (e.g. the and food-borne trematodiases with more than 250 Drugs for Neglected Diseases Initiative (DNDi) million infections (Keiser and Utzinger, 2005; focusing on human African trypanosomiasis and Steinmann et al. 2006). Whilst the global burden of leishmaniasis), devoted drug discovery and devel- schistosomiasis has been estimated at 1.7–4.5 million opment programmes do not yet exist for any of the disability-adjusted life years (Utzinger and Keiser, major helminth diseases (Ridley and Kita, 2007). 2004; Hotez et al. 2009), that of food-borne trema- Moreover, funding for basic research on these para- todiases remains to be investigated (Keiser and sites and the pathogenesis of neglected tropical dis- Utzinger, 2009). Schistosomiasis and food-borne eases has been inadequate (Renslo and McKerrow, trematodiases belong to the so-called neglected 2006). To date, in vitro cultivation of trematodes tropical diseases (Hotez et al. 2009; Keiser and lags behind the cultivation of protozoa or bacteria Utzinger, 2009). The global strategy for the control and cultivation throughout the entire life cycle is not of schistosomiasis and food-borne trematodiases and possible (Smyth and Halton, 1983). Additionally, other parasitic worm infections is morbidity control only very few digeneans are maintained in the lab- oratory, primarily due to their complex life cycles. * Corresponding author: Tel: +41 61 284-8218; Fax: Life cycles requiring at least 2 hosts, a vertebrate +41 61 284-8105. E-mail: [email protected] and a molluscan host, are the rule among digeneans Parasitology (2010), 137, 589–603. f Cambridge University Press 2009 doi:10.1017/S0031182009991739 Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:55:12, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182009991739 J. Keiser 590 (Cox, 1993; Gryseels et al. 2006; Keiser and S. haematobium is much less studied, as it is diffi- Utzinger, 2009). Finally, though target-based tre- cult to grow in rodents (Doenhoff et al. 2009). To matodicidal drug discovery is starting to bear fruit my knowledge, the life cycle of S. haematobium (Caffrey, 2007; Sayed et al. 2008; Abdulla et al. is currently maintained only in two laboratories, 2009), translation of targets identified through com- namely the Theodor Bilharz Research Institute parative genome searches and microarray analysis (Giza, Egypt) and the Schistosomiasis Resource into validated targets will require substantial econ- Center. ‘Sibling’ species of S. haematobium, such as omic efforts (Renslo and McKerrow, 2006). S. bovis, S. matthei or S. margrebowiei, the life cycles In the present article, I review in vitro and in vivo of which can be maintained in laboratory rodents, trematode models available for chemotherapeutic might serve as models for S. haematobium (Agnew studies. Emphasis is placed on screening against et al. 1989). whole parasites since a molecular-target approach is S. japonicum, the third major human schistosome still rarely employed in trematodicidal drug dis- species, is mainly studied in China. Nonetheless covery. The focus is on a blood fluke (Schistosoma several institutions outside China maintain the life mansoni), a liver fluke (Fasciola hepatica) and an in- cycle and infected snails and mammals are also avail- testinal fluke (Echinostoma caproni). While S. man- able on request from the Schistosomiasis Resource soni and F. hepatica are major human pathogens, Center. Though less frequently used, schistosome E. caproni is a rodent and avian fluke, which is widely species infecting other species of definitive hosts and effectively used as a laboratory model. Examples might also prove useful for experimental studies: for of in vitro and in vivo evaluation of compounds example, the bird schistosome Trichobilharzia ocel- for activity against these three selected flukes are lata reaches oviposition after 9 days already and is given. I conclude that for better targeted future not pathogenic. Its life cycle has been described as trematodicidal drug discovery there is a strong need troublesome (Smyth and Halton, 1983). to develop validated, robust high-throughput in vitro systems with simple readouts. S. mansoni in vitro assay based on schistosomula SCHISTOSOMA MANSONI Following the establishment of the S. mansoni life cycle in the laboratory, in vitro parasite culture S. mansoni is an important model to study techniques were developed (Ramirez et al. 2007). schistosomiasis Early work with schistosomula was based on the re- S. mansoni is the most widely used schistosome covery of young worms from the lungs of infected model, and its life cycle is kept in many institutions rodents, hence only limited worm material was worldwide. Fig. 1 summarizes laboratories in available (Smyth and Halton, 1983). The discovery Europe, USA, South America, Asia and Northern that schistosomula can be obtained by transforming Africa, which currently maintain the life cycle of cercariae using simple techniques as centrifugation, S. mansoni. Several of these laboratories such as repeated aspiration through a syringe needle or the Schistosomiasis Resource Center (Biomedical chemical stimulation was a breakthrough in the field Research Institute; Bethesda, USA) or the Theodor of schistosome cultivation. Today cercariae are often Bilharz Research Institute, Giza, Egypt also provide used as starting material for schistosome in vitro schistosome material for research or teaching pur- studies as large numbers of schistosomula can be poses. Remarkably, our search did not identify any obtained in a cost-effective manner (Table 1, Fig. 2) laboratories in sub-Saharan Africa (the area con- (Smyth and Halton, 1983; Abdulla et al. 2009; sidered to be most severely affected by schistosome- Caffrey et al. 2009). In addition, most importantly, induced morbidity (van der Werf et al. 2003), which the use of mechanically obtained schistosomula maintain the complete laboratory life-cycle of reduces and replaces the use of live animals in S. mansoni. accordance with the 3Rs (reduce, replace, refine) Briefly, in the definitive host S. mansoni worms of animal protection principles (Broadhead and develop from a post-penetration larval stage, the Bottrill, 1997). An assay with artificially produced schistosomulum. The female worms produce eggs schistosomula might serve as a pre-screen in drug which leave the body in excreta – faeces in the case of sensitivity assays, however one has to keep in mind S. mansoni, and on contact of
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