Recent Advances in the Biology of Echinostoma species in the “revolutum” Group

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Abstract

This review examines the significant literature on the biology of Echinostoma species in the “revolutum” group. We have considered 10 species belonging to this group. There is a considerable body of literature for four of the species, i.e. Echinostoma caproni, E. trivolvis, E. paraensei and E. revolutum. For these species we have arranged coverage to include the following headings: (1) systematic and descriptive studies; (2) experimental, manipulative and ecological studies; (3) physiological and biochemical studies; (4) immunological and molecular studies. For the remaining six species, i.e. E. friedi, E. miyagawai, E. echinatum, E. parvocirris, E. luisyrei and E. jurini, the literature is not very extensive, and headings were not used. Considerable information in various areas of modern parasitology can be obtained from species in the “revolutum” complex for which the entire life cycle is maintained in the laboratory. The review includes a list of researchers and their addresses who currently maintain such life cycles.

Introduction

The purpose of this review is to examine the significant literature on Echinostoma species in the “revolutum” group. The criteria used for distinguishing species in this group have been discussed in a recent “critical comments’ article by Fried and Toledo (2004). The systematics of the echinostomes within the 37-collar spined “revolutum” group have long been confused. For this review, we recognize the nine species listed in Table 3 of the review by Kostadinova and Gibson (2000). The valid species in this group and the number of citations listed in the ISI Web of Science from 1988 to 2004 are as follows: Echinostoma caproni (137); E. trivolvis (92); E. paraensei (73); E. revolutum (63); E. friedi (4); E. miyagawai (3); E. echinatum (2); E. parvocirrus (1); E. jurini (0). We recognize the fact that some of these citations are only tangentially related to studies on the species indicated, so the number of ISI citations is greater than the literature directly concerned with each species. We also recognize one other species, E. luisreyi, recently described by Maldonado et al. (2003) to belong to this group. As of February 2004, this species has only one citation in the ISI.

Some reviews on the biology of echinostomes are as follows: Huffman and Fried (1990) reviewed a significant earlier literature on Echinostoma and echinostomiasis to about 1988 and covered the salient material on E. caproni, E. trivolvis, E. paraensei, E. revolutum and E. echinatum. The papers cited in the Huffman and Fried (1990) review on species in the “revolutum” complex have not been examined in this review. Likewise, 72 of the 137 citations on E. caproni mentioned in an ISI were covered in earlier review on E. caproni by Fried and Huffman (1996) and are not examined here.

The edited book by Fried and Graczyk (2000) also serves as a background for this review. The literature covered in that book was mainly through 1998 and the book is not organized on a species basis. Coverage of echinostomes in the “revolutum” group was not a major theme of the book which emphasized the use of echinostomes as experimental models.

In this review, coverage of each species is done following the format of Fried (2001), where the coverage was limited to the most important genera of echinostomes, except the Echinostoma. Such coverage for each species for which there is sufficient literature includes the following: (1) systematic and descriptive studies; (2) experimental, manipulative and ecological studies; (3) physiological and biochemical studies; (4) immunological and molecular studies. The coverage is done based on the number of citations (from highest to lowest) for each species according to the ISI Web Search from 1988–2004 and is as follows: E. caproni; E. trivolvis; E. paraensei; E. revolutum; E. friedi; E. miyagawai; E. echinatum; E. parvocirrus; E. luisreyi; E. jurini. Where the citations are limited, the coverage is mainly on their systematic and descriptive studies.

Some of the species in the “revolutum” group are useful models for basic and applied research in modern parasitology. This is particularly true for E. caproni, E. trivolvis, E. revolutum, E. paraensei and E. friedi where their life cycles are maintained in various laboratories, worldwide. A coverage of these species demonstrates their use in modern parasitology.

Section snippets

Systematic and Descriptive Studies

Systematic and descriptive studies were scant and primarily concerned with the developmental stages of Echinostoma caproni. Ataev et al. (2001) characterized the germinal elements and their development in E. caproni and E. paraensei miracidia. Ataev et al. (1998) also described in vivo and in vitro development of mother oocysts of E. caproni using B. glabrata snails and embryonic cell lines. Iomini and Justine (1997) provided transmission and scanning electron microscopy evidence of

Systematic and Descriptive Studies

Kanev et al. (1995a) completed the life cycle of Echinostoma trivolvis (Cort, 1914) experimentally and discussed the validity and identity of this species. They provided a list of the synonyms for cercariae and adults of E. trivolvis. The first intermediate host of this echinostome is the planorbid snail Helisoma trivolvis, and the second intermediate hosts are various pulmonate and prosobranch snails, bivalves, planarians, fishes, frogs and tadpoles. Various birds and mammals serve as the

Systematic and Descriptive Studies

Lie and Basch (1967) described the intramolluscan stages of Echinostoma paraensei from Biomphalaria glabrata collected in Brazil; they also described the adult stage of this echinostome from the experimentally infected hamsters, albino rats and mice. Maldonado et al. (2001a) identified the only known natural host of the adult worm as the rodent Nectomys squamipe. The life cycle of this 37-collar-spined echinostome can be maintained in the laboratory using B. glabrata snails as intermediate

Systematic and Descriptive Studies

Considerable work in the past 12 years has been done on faunistic studies of Echinostoma revolutum from naturally infected hosts. This work is summarized as follows: Brasil and Amato (1992) recovered E. revolutum for the first time in the sparrow, Passer domesticus, in Brazil; Kulisic and Lepojev (1994) reported E. revolutum from wild ducks, Anas platyrhynchos, in Belgrade, Yugoslavia; Sitko (1998) found this echinostome in birds of prey (Falconiformes) in the Czech Republic; the falcon, Buteo

Echinostoma Friedi

Toledo et al. (2000) first described Echinostoma friedi as a distinct 37-collar-spined species of the “revolutum” group. The freshwater snail, Lymnaea peregra, is the natural first and second intermediate host, and L. corvus and Gyraulus chinensis serve as experimental first and second intermediate hosts. The natural definitive host is Rattus norvegicus and albino rats, golden hamsters and chicks are suitable experimental hosts.

Several subsequent studies examined the life cycle stages of E.

Echinostoma Miyagawai

Kostadinova (1999) described and figured the chaetotaxy of the cercaria of Echinostoma miyagawai (Ishii, 1932) obtained from Planorbis planorbis, a brackish water snail in Bulgaria. Comparisons of the sensory patterns of this cercariae with those of E. revolutum, E. trivolvis, E. caproni and other 37-collar spined forms showed the distinct species status of E. miyagawai which shows a unique number and distribution of certain sensory groups. The utility and limitations of using chaetotaxy to

Echinostoma Echinatum

Kostadinova and Gibson (2000) considered Echinostoma echinatum (Zeder, 1803) as a valid species within the “revolutum” group. Synonyms for this species are E. lindoense Sandground and Bonne, 1940; E. barbosai Lie and Basch, 1966; and Cercaria spinifera La Valetta, 1855. The geographical distribution for this species is Europe, Asia and South America and definitive hosts can be birds or mammals. Various first intermediate snail hosts have been described for this echinostome including species of

Echinostoma Parvocirrus

Nassi and Dupouy (1988) described this 37-collar spined form as a new species, Echinostoma parvocirrus, isolated from the naturally infected Biomphalaria glabrata snails in Guadeloupe, French West Indies. This planorbid serves as both the first and the second intermediate host for this echinostome and only birds appear to serve as definite hosts. The number of penetration gland pores on the cercaria is six; the total number of paraesophageal gland pores on the cercaria is 24, different from any

Echinostoma Luisreyi

Maldonado et al. (2003) described the life cycle of a new 37-collar spined species in the “revolutum” group from Brazil and named it Echinostoma luisreyi. This is the only species included in our coverage but not mentioned in Kostadinova and Gibson (2000). The natural first snail intermediate host of this species is Physa marmorata. The physid and Biomphalaria glabrata serve as experimental second intermediate hosts. The worm recovery rate for experimental infections in mice and hamsters was

Echinostoma Jurini

Kanev et al. (1995b) has redescribed the life cycle of Echinostoma jurini. Their experimental studies showed that the first intermediate host is a viviparid snail; the second intermediate hosts are the molluscs, frogs and freshwater turtles and the final hosts are mammals. E. jurini occurs in Europe and possibly in Asia where viviparid snail hosts are distributed.

Concluding Remarks

We have provided salient information on the systematic and descriptive studies; experimental, manipulative and ecological studies; physiological and biochemical studies; and immunological and molecular studies for the four most studied species in the “revolutum” complex, that is, Echinostoma caproni, E. trivolvis, E. paraensei and E. revolutum. The available significant literature on the less studied species in this group, that is, E. friedi, E. miyagawai, E. echinatum, E. parvocirrus, E.

Acknowledgements

We thank Ms. Leena Tamang and Ms. Elizabeth L. Ponder for the editorial assistance and literature retrieval. We are especially grateful to Ms. Jessica L. Schneck for her help in literature retrieval, editing and typing the manuscript.

References (190)

  • J.E. Humphries et al.

    Infectivity and growth of Echinostoma revolutum (Froelich, 1802) in the domestic chick

    International Journal for Parasitology

    (1997)
  • C. Iomini et al.

    Spermiogenesis and spermatozoon of Echinostoma caproni (Platyhelminthes, Digenea): transmission and scanning electron microscopy, and tubulin immunocytochemistry

    Tissue & Cell

    (1997)
  • S.L. Iorio et al.

    Concurrent infections of Echinostoma caproni and Echinostoma trivolvis in ICR mice

    International Journal for Parasitology

    (1991)
  • M. Korner et al.

    Chemo-orientation of echinostome cercariae towards their snail hosts: Amino acids signal a low host-specificity

    International Journal for Parasitology

    (1998)
  • C.M. Adema et al.

    A time lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa

    Journal of Parasitology

    (1994)
  • C.M. Adema et al.

    Evidence from two planorbid snails of a complex and dedicated response to digenean (echinostome) infection

    Parasitology

    (1999)
  • C.M. Adema et al.

    A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection

    Proceedings of the National Academy of Science USA

    (1997)
  • B.K. Albrecht et al.

    Effects of Echinostoma caproni infection on the phospholipid and sphingolipid content of the intestinal mucosa of ICR mice

    Journal of Helminthology

    (1998)
  • K.J. Alden

    Helminths of the opossum, Didelphis virginiana, in southern Illinois, with a compilation of all helminths reported from this host in North America

    Journal of the Helminthological Society of Washington

    (1995)
  • G.L. Ataev et al.

    Cellular response to Echinostoma caproni infection in Biomphalaria glabrata strains selected for susceptibility resistance

    Development and Comparative Immunology

    (1999)
  • G.L. Ataev et al.

    Germinal elements and their development in Echinostoma caproni and Echinostoma paraensei (Trematoda) miracidia

    Journal of Parasitology

    (2001)
  • G.L. Ataev et al.

    Comparison of Echinostoma caproni mother sporocyst development in vivo and in vitro using Biomphalaria glabrata snails and a B-glabrata embryonic cell line

    Journal of Parasitology

    (1998)
  • J. Baek et al.

    Zinc deficiency and host response to helminth infection: Echinostoma caproni infections in CBA mice

    Journal of Helminthology

    (1996)
  • C.D. Balfour et al.

    Effects of a 100 metacercarial cyst inoculum on the host-parasite relationship of Echinostoma caproni and ICR mice

    Journal of Helminthology

    (2001)
  • P.C. Beaver

    Experimental studies on Echinostoma revolutum (Froelich) a fluke from birds and mammals

    Illinois Biological Monographs

    (1937)
  • F.H.M. Borgsteede et al.

    A study of the helminth fauna of birds belonging to the Passeriformes in the Netherlands

    Acta Parasitologica

    (2000)
  • F.H.M. Borgsteede et al.

    The helminth fauna of birds of prey (Accipitriformes, Falconiformes, and Strigiformes) in the Netherlands

    Acta Parasitologica

    (2003)
  • M.D. Brasil et al.

    Faunistic analysis of the helminths of sparrows (Passer domesticus L, 1758) captured in Campo Grande, Rio de Janeiro, R.J

    Memorias do Instituto Oswaldo Cruz

    (1992)
  • L.R. Brunett et al.

    Immune responses during the acute stages of infection with the intestinal trematode Echinostoma caproni

    Parasitology

    (2000)
  • C.A. Conaway et al.

    High performance thin layer chromatographic analysis of sugars in Helisoma trivolvis (Pennsylvania strain) infected with larval Echinostoma trivolvis and in uninfected H. trivolvis (Pennsylvania and Colorado strains)

    Journal of Planar Chromatography-Modern TLC

    (1995)
  • M.R. Daras et al.

    Effects of a high-carbohydrate diet on growth of Echinostoma caproni in ICR mice

    Comparative Parsitology

    (2000)
  • V. Dimitrov et al.

    Argentophilic structures of the miracidium of Echinostoma trivolvis (Cort, 1914) (Trematoda, Echinostomatidae)

    Journal of Parasitology

    (1995)
  • V. Dimitrov et al.

    Sensillae of the cercariae of Echinostoma trivolvis (Cort, 1914) (Trematoda: Echinostomatidae)

    Parasite

    (1997)
  • D.M. Ford et al.

    The effects of salinity, pH and temperature on the half-life and longevity of Echinostoma caproni miracidia

    Journal of Helminthology

    (1998)
  • D.J. Forrester et al.

    Parasitic helminths and arthropods of fulvous whistling ducks (Dendrocygna bicolor) in southern Florida

    Journal of the Helminthological Society of Washington

    (1994)
  • B.A. Frazer et al.

    Host–parasite relationships between Echinostoma caproni and RAG-2-deficient mice

    Parasitology Research

    (1999)
  • B. Fried et al.

    Light and scanning electron microscopic observations of the daughter rediae of Echinostoma trivolvis (Trematoda)

    Parasitology Research

    (1992)
  • Fried, B. and Graczyk, T.K. (eds.) (2000). Echinostomes as Experimental Models for Biological Research, p. 273....
  • B. Fried et al.

    Effects of larval Echinostoma caproni and Schistosoma mansoni infection on the heart rate of Biomphalaria glabrata snail

    Veliger

    (2003)
  • B. Fried et al.

    In vitro and in vivo encystment of the cercariae of Echinostoma caproni

    Journal of Parasitology

    (2002)
  • B. Fried et al.

    Use of an acetocarmine procedure to examine the excysted metacercariae of Echinostoma caproni and Echinostoma trivolvis

    Journal of Helminthology

    (1992)
  • B. Fried et al.

    Effects of snail-conditioned water from Biomphalaria glabrata on hatching of Echinostoma caproni miracidia

    Parasitology Research

    (1999)
  • B. Fried et al.

    Exposure of Dugesia tigrina (Turbellaria) to cercariae of Echinostoma trivolvis and Echinostoma caproni (Trematoda)

    Journal of Parasitology

    (1991)
  • Fried, B. and Toledo, R. (2004). Criteria for species determination in the “revolutum” group of Echinostoma. Journal of...
  • B. Fried et al.

    Thin layer chromatographic analysis of beta-carotene and lutein in Echinostoma trivolvis (Trematoda) rediae

    Journal of Parasitology

    (1993)
  • B. Fried et al.

    Fatty acid composition of Echinostoma trivolvis (Trematoda) rediae and adults and of the digestive gland-gonad complex of Helisoma trivolvis (Gastropoda) infected with the intramolluscan stages of this echinostome

    Parasitology Research

    (1993)
  • B. Fried et al.

    Experimental infection of juvenile Biomphalaria glabrata with cercariae of Echinostoma trivolvis

    Journal of Parasitology

    (1995)
  • B. Fried et al.

    Chemoattraction and penetration of Echinostoma trivolvis and E. caproni cercariae in the presence of Biomphalaria glabrata, Helisoma trivolvis, and Lymnaea elodes dialysate

    Parasitology Research

    (1997)
  • B. Fried et al.

    Maintenance of the life cycle of Echinostoma trivolvis (Trematoda) in dexamethasone-treated ICR mice and laboratory-raised Helisoma trivolvis (Gastropoda)

    Parasitology Research

    (1997)
  • B. Fried et al.

    Experimental infection of Rana pipiens tadpoles with Echinostoma trivolvis cercariae

    Parasitology Research

    (1997)
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