ReviewThe early stages of Echinococcus granulosus development
Introduction
Human cystic echinococcosis (CE) is a cyclozoonotic infection produced by the larval stage (metacestode) of Echinococcus granulosus. It has a world-wide distribution with endemic foci in each inhabited continent (Matossian et al., 1977; Rausch, 1986; Eckert and Thompson, 1988; Schantz et al., 1995) and constitutes a major economic and health problem (McManus and Smyth, 1986; Schwabe, 1986).
The knowledge of post-oncospheral differentiation is essential for the comprehension of the host-parasite relationship since structural changes of the developing hydatid cyst tegument may reflect the parasite's immunoprotective mechanism (Holcman et al., 1994). In CE, the oncosphere of E. granulosus plays a central role in research on echinococcosis control. The oncosphere is the first invasive form recognized by the intermediate host's immune reactions and becomes also a target of the early responses. Since oncosphere that develop into cyst must evade the host immune system, ultrastructural studies of the tegumentary differentiation may elucidate the survival mechanism of the parasite.
The tegument is a complex living structure involved in penetration of the host intestine, absorption of nutrients, and stimulation of the host immune response (protective antibodies are active on the microvilli of the metacestodes). The essential host-parasite interface is at the parasite plasma membrane, and it is the immune recognition at this site that must initiate the parasite rejection by whatever mechanism (Ortega-Pierres et al., 1984). The plasma membrane of oncospheral epithelium is the obvious site of both functional antigen expression and of complement-mediated lysis in the host (Heath et al., 1994). It has been shown that successful immunoprophylaxis is feasible on the basis of oncosphere-derived antigens (Heath, 1986, Heath, 1995).
Section snippets
Development from the egg to an oncosphere
The following review is based on the ultrastructure of epithelial changes during the first 5 (Holcman et al., 1994) and 8 (Harris et al., 1989) days of the E. granulosus development. Figures are taken from Holcman et al. (1994).
Mature E. granulosus eggs have a thick embryophore and its ultrastructure shows it is made of thick elongated blocks united by electron-lucid cement (Fig. 1) and the oncosphere membrane is a thin cytoplasmic layer surrounding the oncosphere. In the hatched oncosphere (
Post-oncospheral development
The post-oncospheral development is a complex process of cytodifferentiation difficult to be observed in vivo.
There is a great number of studies on in vitro culture of protoscoleces from fertile hydatid cysts to adult strobilate stage and a significant number on the ultrastructure of E. granulosus protoscolex tegument and of the germinal and laminated layers of the hydatid cyst (Morseth, 1967; Bortoletti and Ferretti, 1973, Bortoletti and Ferretti, 1978; Lascano et al., 1975; Conder et al., 1983
The mature cyst
The developed metacestode is an unilocular cyst and could attain large size. The cavity of the cyst is filled with sterile hydatid fluid, which is a complex mixture of parasite-derived molecules and host-derived serum components (reviewed by Rickard and Lightowlers, 1986; McManus and Bryant, 1995). The cyst wall consists of an inner thin multinucleated germinal layer and an outer thick acellular laminated layer. The laminated layer is made up of a number of laminations and besides giving
Conclusions
This review intended to point out that early stages of metacestode development are still scarcely elucidated in the literature. Further studies on morphogenesis of the surface epithelium could lead to a better understanding of the essential aspects of host/parasite relationship in cystic echinococcosis. It was shown that the laminated layer, which is presumed to protect the parasite from the host's immune response, is of parasite origin. Assuming that the Vg secretory vesicles are responsible
References (49)
- Antoniou, M. and Tselentis, Y. (1993) Studies on Echinococcus Granulosus using the scanning electron microscope....
- Bortoletti, G. and Ferretti, G. (1973) Investigation on larval forms of Echinococcus granulosus with electron...
- Bortoletti, G. and Ferretti, G. (1978) Ultrastructural aspects of fertile and sterile cysts of Echinococcus granulosus...
- Casado, N., Criado, A., Jimenez, A., De Armas, C., Brasa, C., Perez-Serrano, J. and Rodriguez-Caabeiro, F. (1992)...
- Coltorti, E.A. and Varela-Dı́az, V.M. (1974) Echinococcus granulosus: penetration of macromolecules and their...
- Coltorti, E.A. and Varela-Dı́az, V.M. (1975) Penetration of host IgG molecules into hydatid cyts. Z. Parasitenkd. 48,...
- Conder, G.A., Marchiondo, A.A., Williams, F. and Andersen, F.L. (1983) Freeze-etch characterization of the teguments of...
- Eckert, J. and Thompson, R.C.A. (1988) Echinococcus strains in Europe (review). Trop. Med. Parasitol. 39,...
- Fairweather, I. and Threadgold, L.T. (1981) Hymenolepis nana: the fine structure of the `penetration gland' and nerve...
- Gottstein, B. and Felleisen, R. (1995) Protective immune mechanism against the metacestode of Echinococcus...
Cited by (33)
A possible Echinococcus granulosus calcified cyst found in a medieval adult female from the churchyard of Santo Domingo de Silos (Prádena del Rincón, Madrid, Spain)
2017, International Journal of PaleopathologyCitation Excerpt :The Christian Reconquer, in 1085, does not change the previous livestock activity (Puñal, 1988), and later King Alfonso VIII regulated sheep farming in his 1202 jurisdiction (Sánchez, 1982). According to Holcman and Heath (1997), the close contact between herds and humans increases the likelihood of cyclozoonotic infection. Today, it is known that hydatidosis is a condition found across every continent (Eckert et al., 2000; WHO, 2015), with the exception of Antarctica (WHO, 2015).
Laboratory Diagnosis of Echinococcus spp. in Human Patients and Infected Animals
2017, Advances in ParasitologyCitation Excerpt :The LL is a structure rich in carbohydrates, constituting a specialized extracellular matrix that is only found in Echinococcus. The LL begins to be secreted by the oncosphere when reaching a target organ in the intermediate host, being in these first steps of development similar to the mature LL in fully developed cysts already at 14–20 days post infection (after egg ingestion; Holcman and Heath, 1997). The structure consists of fibrils and dense granules, the later only present in the cysts of E. granulosus.
Biology and Systematics of Echinococcus
2017, Advances in ParasitologyCitation Excerpt :When ingested by a suitable intermediate host, viable eggs of Echinococcus hatch in the stomach and small intestine. Hatching is a two-stage process involving (1) the passive disaggregation of the embryophoric blocks in the stomach and intestine and (2) the activation of the oncosphere and its liberation from the oncospheral membrane (reviewed by Holcman and Heath, 1997; Jabbar et al., 2010; Lethbridge, 1980). Disaggregation of the embryophoric blocks appears to require the action of proteolytic enzymes, including pepsin and pancreatin, in the stomach and/or intestine but does not depend on any one specific enzyme.
Echinococcus as a model system: Biology and epidemiology
2014, International Journal for ParasitologyCitation Excerpt :The origin of the laminated layer was controversial for some time, i.e. whether it is entirely of parasite origin or if there is a host contribution. Holcman and Heath (1997) demonstrated that it is entirely of parasite (germinal layer) origin by studying the early stages of cyst development from oncospheres in vitro. Considerable metabolic activity in the germinal layer is required to synthesise and maintain the interfacial barrier of the laminated layer (Parkinson et al., 2012).
Echinococcosis
2011, Tropical Infectious Diseases: Principles, Pathogens and PracticeEchinococcosis
2011, Tropical Infectious Diseases