Adaptation of Lymnaea fuscus and Radix balthica to Fasciola hepatica through the experimental infection of several successive snail generations

Particle and Fibre Toxicology

Gilles Dreyfuss²  Abdeslam Mekroud¹  Philippe Vignoles²  Amal Titi¹  Daniel Rondelaud² 

[1] PADESCA Laboratory, Veterinary Science Institute, University Constantine 1, El Khroub 25100, Algeria;INSERM 1094, Faculties of Medicine and Pharmacy, Limoges 87025, France

关键词: Redia;    Radix balthica;    Prevalence;    Lymnaea fuscus;    Galba truncatula;    Fasciola hepatica;    Experimental infection;    Cercaria;   

Others  :  819449
DOI  :  10.1186/1756-3305-7-296

 received in 2014-02-25, accepted in 2014-06-17,  发布年份 2014

【 摘 要 】

Background

High prevalence of Fasciola hepatica infection (>70%) was noted during several outbreaks before the 2000s in several French farms where Galba truncatula is lacking. Other lymnaeids such as Lymnaea fuscus, L. glabra and/or Radix balthica are living in meadows around these farms but only juvenile snails can sustain complete larval development of F. hepatica while older snails were resistant. The low prevalence of infection (<20%) and limited cercarial production (<50 cercariae per infected snail) noted with these juveniles could not explain the high values noted in these cattle herds. As paramphistomosis due to Calicophoron daubneyi was not still noted in these farms, the existence of another mode of infection was hypothesized. Experimental infection of several successive generations of L. glabra, originating from eggs laid by their parents already infected with this parasite resulted in a progressive increase in prevalence of snail infection and the number of shed cercariae. The aim of this paper was to determine if this mode of snail infection was specific to L. glabra, or it might occur in other lymnaeid species such as L. fuscus and R. balthica.

Methods

Five successive generations of L. fuscus and R. balthica were subjected to individual bimiracidial infections in the laboratory. Resulting rediae and cercariae in the first four generations were counted after snail dissection at day 50 p.e. (20°C), while the dynamics of cercarial shedding was followed in the F5 generation.

Results

In the first experiment, prevalence and intensity of F. hepatica infection in snails progressively increased from the F1 (R. balthica) or F2 (L. fuscus) generation. In the second experiment, the prevalence of F. hepatica infection and the number of shed cercariae were significantly lower in L. fuscus and R. balthica (without significant differences between both lymnaeids) than in G. truncatula.

Conclusion

The F. hepatica infection of several successive snail generations, coming from parents infected with this parasite, resulted in a progressive increase in prevalence and intensity of snail infection. This may explain high prevalence of fasciolosis noted in several cattle-breeding farms when the common snail host of this digenean, G. truncatula, is lacking.

【 授权许可】

   
2014 Rondelaud et al.; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Torgerson P, Claxton J: Epidemiology and control. In Fasciolosis. Edited by Dalton JP. Oxon: CABI Publishing; 1999:113-149.
• [2]Taylor EL: Fascioliasis and the liver-fluke. Volume 64. Rome: FAO Agricultural Studies; 1965.
• [3]Boray JC: Experimental fascioliasis in Australia. Adv Parasitol 1969, 7:95-210.
• [4]Boray JC: The potential impact of exotic Lymnaea spp. on fascioliasis in Australasia. Vet Parasitol 1978, 4:127-141.
• [5]Busson P, Busson D, Rondelaud D, Pestre-Alexandre M: Données expérimentales sur l'infestation des jeunes de cinq espèces de limnées par Fasciola hepatica L. Ann Parasitol Hum Comp 1982, 57:555-563.
• [6]Bouix-Busson D, Rondelaud D: L'infestation de Lymnaea glabra Müller par Fasciola hepatica L. Etude expérimentale sur le terrain. Ann Parasitol Hum Comp 1986, 61:215-225.
• [7]Dreyfuss G, Moukrim A, Rondelaud D, Vareille-Morel C: Several field observations concerning infection of Lymnaea palustris by Fasciola hepatica. J Helminthol 1994, 68:115-118.
• [8]Dreyfuss G, Abrous M, Rondelaud D: The susceptibility of Lymnaea fuscus to experimental infection with Fasciola hepatica. J Parasitol 2000, 86:158-160.
• [9]Dreyfuss G, Vignoles P, Rondelaud D: Variability of Fasciola hepatica infection in Lymnaea ovata in relation to snail population and snail age. Parasitol Res 2000, 86:69-73.
• [10]Vignoles P, Dreyfuss G, Rondelaud D: Redial growth and cercarial productivity of Fasciola hepatica in three species of young lymnaeid snails. J Helminthol 2002, 76:269-272.
• [11]Chipev N, Vassilev I, Samnaliev P: Interactions between Paramphistomum cf daubneyi Dinnik, 1962 and Fasciola hepatica L. in successive cross-invasions of Lymnaea (Galba) truncatula. Helminthologia 1985, 20:80-88.
• [12]Southgate VR, Brown DS, Warlow R, Knowles RJ, Jones A: The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitol Res 1989, 75:381-391.
• [13]Abrous M, Rondelaud D, Dreyfuss G: Paramphistomum daubneyi and Fasciola hepatica: the effect of dual infection on prevalence and cercarial shedding in preadult Lymnaea glabra. J Parasitol 1996, 82:1026-1029.
• [14]Abrous M, Rondelaud D, Dreyfuss G, Cabaret J: Unusual transmission of the liver fluke, Fasciola hepatica, by Lymnaea glabra or Planorbis leucostoma in France. J Parasitol 1998, 84:1257-1259.
• [15]Abrous M, Rondelaud D, Dreyfuss G, Cabaret J: Infection of Lymnaea truncatula and Lymnaea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France. Vet Res 1999, 30:113-118.
• [16]Abrous M, Rondelaud D, Dreyfuss G: A field study of natural infections in three freshwater snails with Fasciola hepatica and/or Paramphistomum daubneyi in central France. J Helminthol 2000, 74:189-194.
• [17]Degueurce F, Abrous M, Dreyfuss G, Rondelaud D, Gevrey J: Paramphistomum daubneyi and Fasciola hepatica: the prevalence of natural or experimental infection in four species of freshwater snails in eastern France. J Helminthol 1999, 73:197-202.
• [18]Rondelaud D: Cressonnières naturelles du Limousin et risques de distomatose humaine à Fasciola hepatica. Ann Sci Limousin 2004, 15:1-14. Published online in Annales Scientifiques du Naturaliste, 2012
• [19]Rondelaud D, Djuikwo-Teukeng FF, Vignoles P, Dreyfuss G: Lymnaea glabra: progressive increase in susceptibility to Fasciola hepatica through successive generations of experimentally-infected snails. J Helmintholin press
• [20]Vareille-Morel C, Dreyfuss G, Rondelaud D: The characteristics of habitats colonized by three species of Lymnaea in swampy meadows on acid soil: their interest for fasciolosis control. Ann Limnol-Int J Limnol 1999, 35:173-178.
• [21]Rondelaud D, Vignoles P, Dreyfuss G: La Limnée tronquée, un mollusque d’intérêt médical et vétérinaire. Limoges: Presses Universitaires du Limousin (PULIM); 2009.
• [22]Novobilský A, Kašný M, Beran L, Rondelaud D, Höglund J: Lymnaea palustris and Lymnaea fuscus are potential but uncommon intermediate hosts of Fasciola hepatica in Sweden. Parasit Vectors 2013, 6:251. BioMed Central Full Text
• [23]Schniebs K, Glöer P, Vinarski MV, Hundsdoerfer AK: Intraspecific morphological and generic diversity in Radix balthica (Linnaeus 1758) (Gastropoda: Basommatophora: Lymnaeidae) with morphological comparison to other European Radix species. J Conchol 2011, 40:657-678.
• [24]Gold D: Growth and survival of the snail Lymnaea truncatula: effects of soil type, culture medium and Fasciola hepatica infection. Isr J Zool 1980, 29:163-170.
• [25]Vignoles P, Rondelaud D, Dreyfuss G: A first infection of Galba truncatula with Fasciola hepatica modifies the prevalence of a subsequent infection and cercarial production in the F1 generation. Parasitol Res 2003, 91:349-352.
• [26]Ollerenshaw CB: Some observations on the epidemiology of fascioliasis in relation to the timing of molluscicide applications in the control of the disease. Vet Rec 1971, 88:152-164.
• [27]Sanabria R, Mouzet R, Courtioux B, Vignoles P, Rondelaud D, Dreyfuss G, Cabaret J, Romero J: Intermediate snail hosts of French Fasciola hepatica: Lymnaea neotropica and Lymnaea viatrix are better hosts than local Galba truncatula. Parasitol Res 2012, 111:2011-2016.
• [28]Vignoles P, Novobilský A, Höglund J, Kašný M, Pankrác J, Dreyfuss G, Pointier JP, Rondelaud R: Lymnaea cubensis (Pfeiffer, 1839), an experimental intermediate host for Fascioloides magna. Folia Parasitol 2014, 61:185-188.
• [29]Préveraud-Sindou M, Dreyfuss G, Rondelaud D: Comparison of the migrations of Fasciola hepatica sporocysts in Lymnaea truncatula and other related snail families. Parasitol Res 1994, 80:342-346.
• [30]Préveraud-Sindou M, Rondelaud D: Localization and outcome of Fasciola hepatica sporocysts in Lymnaea truncatula subjected to mono- or plurimiracidial exposures. Parasitol Res 1995, 81:265-267.
• [31]Rondelaud D, Fousi M, Vignoles P, Moncef M, Dreyfuss G: Optimization of metacercarial production for three digenean species by the use of Petri dishes for raising lettuce-fed Galba truncatula. Parasitol Res 2007, 100:861-865.
• [32]Rondelaud D: Données épidémiologiques sur la distomatose humaine à Fasciola hepatica L. dans la région du Limousin, France. Les plantes consommées et les limnées vectrices. Ann Parasitol Hum Comp 1980, 55:393-405.
• [33]Rondelaud D, Dreyfuss G, Bouteille B, Dardé ML: Changes in human fasciolosis in a temperate area. About some observations over a 28-year period in central France. Parasitol Res 2000, 86:753-757.
• [34]Bouix-Busson D, Rondelaud D, Prevost J: Influence du nombre de miracidiums et de l'âge du Mollusque sur la survie et le degré d'infestation de Lymnaea glabra Müller par Fasciola hepatica L. Ann Parasitol Hum Comp 1983, 58:347-352.
• [35]Bouix-Busson D, Rondelaud D, Barthe D: Experimental infection of Lymnaea glabra and L. truncatula by Fasciola hepatica. J Parasitol 1984, 70:1002-1003.
• [36]Bouix-Busson D, Rondelaud D, Combes C: L'infestation de Lymnaea glabra Müller par Fasciola hepatica L. Les caractéristiques des émissions cercariennes. Ann Parasitol Hum Comp 1985, 60:11-21.
• [37]Rondelaud D, Vignoles P, Abrous M, Dreyfuss G: The definitive and intermediate hosts of Fasciola hepatica in the natural watercress beds in central France. Parasitol Res 2001, 87:475-478.
• [38]Jackiewicz M: Błotniarki Europy (Gastropoda: Pulmonata: Lymnaeidae). Poznan: Wydawnictwo Kontekst; 2000.
• [39]Novobilský A, Kašný M, Pankrác J, Rondelaud D, Engström A, Höglund J: Lymnaea fuscus (Pfeiffer, 1821) as a potential intermediate host of Fascioloides magna in Europe. Exp Parasitol 2012, 132:282-286.
• [40]Kendall SB: Snail hosts of Fasciola hepatica in Britain. J Helminthol 1950, 24:63-74.
• [41]Berghen P: Some Lymnaeidae as intermediate hosts of Fasciola hepatica in Belgium. Exp Parasitol 1964, 15:118-124.
• [42]Boray JC: Studies on the relative susceptibility of some lymnaeids to infection with Fasciola hepatica and F. gigantica and on the adaptation of Fasciola spp. Ann Trop Med Parasitol 1966, 60:114-124.
• [43]Sindou P, Rondelaud D, Barthe D: Fasciola hepatica L.: étude comparative de la pathologie viscérale chez six espèces de limnées soumises dès leur naissance à des infestations monomiracidiennes individuelles. Bull Soc Zool Fr 1990, 115:331-340.
• [44]Bargues MD, Vigo M, Horak P, Dvorak J, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S: European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect Genet Evol 2001, 1:85-107.
• [45]Bargues MD, Horak P, Patzner RA, Pointier JP, Jackiewicz M, Meier-Brook C, Mas-Coma S: Insights into the relationships of Palearctic and Nearctic lymnaeids (Mollusca: Gastropoda) by rDNA ITS-2 sequencing and phylogeny of stagnicoline intermediate host species of Fasciola hepatica. Parasite 2003, 10:243-255.
• [46]Bargues MD, Mas-Coma S: Reviewing lymnaeid vectors of fascioliasis by ribosomal DNA sequence analyses. J Helminthol 2005, 79:257-267.
• [47]Mas-Coma S, Valero MA, Bargues MD: Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 2009, 69:41-146.
• [48]Correa AC, Escobar JS, Durand P, Renaud F, David P, Jarne P, Pointier JP, Hurtrez-Bousses S: Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of fascioliasis. BMC Evol Biol 2010, 10:381. BioMed Central Full Text
• [49]Correa AC, Escobar JS, Noya O, Velasquez LE, Gonzalez-Ramirez C, Hurtrez-Bousses S, Pointier JP: Morphological and molecular characterization of Neotropic Lymnaeidae (Gastropoda: Lymnaeoidea), vectors of fasciolosis. Infect Genet Evol 2011, 11:1978-1988.
• [50]Caron Y, Lasri S, Losson B: Fasciola hepatica: an assessment on the vectorial capacity of Radix labiata and R. balthica commonly found in Belgium. Vet Parasitol 2007, 149:95-103.
• [51]Caron Y, Martens K, Lempereur L, Saegerman C, Losson B: New insight in lymnaeid snails (Mollusca, Gastropoda) as intermediate hosts of Fasciola hepatica (Trematoda, Digenea) in Belgium and Luxembourg. Parasit Vectors 2014, 7:66. BioMed Central Full Text
• [52]Szmidt-Adjidé V, Rondelaud D, Dreyfuss G, Cabaret J: The effect of parasitism by Fasciola hepatica and Muellerius capillaris on the nerve ganglia of Lymnaea truncatula. J Invertebr Pathol 1996, 67:300-305.
• [53]de Jong-Brink M: How trematode parasites interfere with reproduction of their intermediate hosts, freshwater snails. J Med Appl Malacol 1990, 2:101-133.