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1. with shedding 68 31 10 without shedding 14 17 11 Frequency of snails with shedding 80 9 64 5 47 6 Patent period onset days 51 2 4 6 50 3 7 2 45 4 2 4 duration days 60 4 23 7 47 3 22 4 30 2 13 3 Shell height at snail s death mm 6 4 1 7 6 1 1 4 6 0 2 3 N of metacercariae derived from 200 initial snails per origin 216 4 52 3 157 8 41 5 54 5 15 8 Percentage of floating cysts 6 4 1 3 5 6 2 3 5 1 3 7 Number of shedding waves 9 8 3 Number of snails that died after the first wave 16 14 8 Duration of the first wave days 3 4 1 6 2 7 2 1 31 3 2 Table 1 The general characteristics of cercarial sheddings in the snail groups infected with miracidia of different origins Parasite 1995 2 275 280 Sk eee 277 25 Percentages Cattle origin 6 Percentages Sheep origin 0 0 0 10 12 14 16 18 20 22 24 2 4 6 8 0 10 12 14 16 18 20 22 24 2 4 6 8 Time classes hours Time classes hours 50 Percentages Rabbit origin 0 0 10 12 14 16 18 20 22 24 2 4 6 8 Time classes hours Fig 1 Numerical distribution of cercariae shed in Z truncatula infected with miracidia of three origins cattle sheep or rabbit during the day Number of rediae cattle sheep rabbit Experimental groups Cl a EN 3 E Fig 2 Numerical distribution of F hepatica rediae in L truncatula infected with miracidia of three origins Abbreviations A degenera
2. SUR LES CARACT RISTIQUES DE L INFESTATION CHEZ LE MOLLUSQUE LYMNAEA TRUN CATULA Des observations ont t r alis es chez lymnaea truncatula afin de d terminer l existence de modifications dans la charge r dienne et les missions cercariennes lorsque la m me population de limn es est expos e des miracidiums qui proviennent d ufs r colt s chez des bovins des ovins ou des lapins infest s naturellement vivant sur les m mes exploitations Des limn es hautes de 4 mm ont t expo s es chacune deux miracidiums par mollusque avant d tre le v es 20 C pendant 30 jours La pr valence de l infestation est de 35 66 et 86 respectivement dans les groupes lapin ovin et bovin par rapport au nombre de survivants au 30 jour Des cer caires ont t mises par les mollusques des trois groupes mais le nombre total de cercaires est plus faible dans le groupe lapin que dans les deux autres 54 5 par mollusque au lieu de 157 8 et 216 4 respectivement Le rythme circadien dans les missions cer cariennes est aussi chang dans le groupe lapin avec des mis sions maximales entre 4 et 8 heures L examen histologique de mollusques infest s montre que le nombre total de r dies est plus faible au 30 jour dans le groupe lapin que dans les deux autres groupes 21 3 par limn e au lieu de 38 4 et 43 7 respectivement Les r dies ind pendantes et d g n r es sont plus nombreuses dans le premier groupe L esp ce de l h
3. of cercarial sheddings were the num ber of snails that shed cercariae the onset and the duration of the patent period the post mortem shell height the total number of metacercariae the percen tage of floating cysts calculated in relation to the total number of metacercariae the number of shed ding waves the number of snails that died after the first wave and the duration of this first wave Lastly we also considered the different time periods of one hour each for which cercaria production was maxi mal Quantification of the total number of rediae depen dent rediae degenerated free rediae recognized by flattened often triangular and pycnotic nuclei of morulae or procercarial embryos and live free rediae was performed at day 30 by histological exa mination of the serial sections Redial maturity was determined by the presence of cercariae and procer cariae and was expressed as a percentage in relation to the total number of live independent rediae Mean values and standard deviations were determi ned in each group for the different parameters They were also calculated for the number of cercariae recorded in the time periods The mean values were subjected to Anova or to the comparison test of expe rimental frequencies Stat Itcf 1987 RESULTS t day 30 the number of surviving snails was respectively 170 156 and 108 in the cattle sheep or rabbit infected groups out of 200 snails per group initially ex
4. than in the rabbit group 3 waves Eighty percent of the snails died after the first shedding wave in the rabbit group whereas only 23 5 died in the cattle group and 45 1 in the sheep group Lastly there were no significant differences in the mean duration of the first wave between the three groups Figure 1 gives the distribution of the number of cer cariae in relation to the different time periods during the day Sheddings were maximal between midnight and 1 a m and between midnight and 2 a m respec tively in the sheep and cattle groups In the rabbit group the period of maximal shedding was different occurring from 4 to 8 a m REDIAL BURDEN AT DAY 30 The total number of rediae was 21 3 10 7 in the rabbit group 38 4 8 4 in the sheep group and 43 7 10 9 in the cattle group A significant difference in the mean values between the rabbit group and the two others was noted F 23 1 p lt 0 001 it was not significant between the two latter groups Figure 2 demonstrates that degenerated free rediae were more numerous in the rabbit group than in the sheep and cattle groups a mean of 12 7 instead of 8 6 and 9 9 respectively A significant difference in the mean values between the rabbit group and those of the other two groups was noted F 11 03 p lt Groups Miracidia of F hepatica Cattle origin Sheep origin Rabbit origin Number of snails with live parthenitae 84 48 21
5. 986 Pages and Th ron 1990 in the cercarial sheddings of Schistosoma sp using hybridization of different tre matode species or of different strains for the same trematode species do not apply to our result in the rabbit group because the three strains of miracidia originated from definitive hosts from the two farms The most likely hypothesis would be to assume that a disturbance in cercarial sheddings occurs whose nature has yet to be elucidated REFERENCES AUDOUSSET J C RONDELAUD D DREYFUSS G amp VAREILLE MOREL C Les missions cercariennes de Fasciola hepatica L chez le mollusque Lymnaea truncatula M ller pro pos de quelques observations chronobiologiques Bulletin de la Soci t Fran aise de Parasitologie 1989 7 217 224 Boray J C Studies on the relative susceptibility of some Parasite 1995 2 275 280 M moire 279 lymneids to infection with Fasciola hepatica and F gigantica and on the adaptation of Fasciola spp Annals of tropical Medicine and Parasitology 1966 60 114 124 Boray J C Experimental fascioliasis in Australia Advances in Parasitology 1969 7 95 210 Boray J C The potential impact of exotic Lymnaea spp on fascioliasis in Australasia Veterinary Parasitology 1978 4 127 141 EuzeBy J Les maladies vermineuses et leurs incidences sur la pathologie humaine Tome II Section 2 Book 1 Vigot fr res ed Paris 1971 798 p HAROUN E M amp HILLYER G V Resistance to fasci
6. Article available at fitip www parasite journal org or pttp FASCIOLA HEPATICA THE INFLUENCE OF THE DEFINITIVE HOST ON THE CHARACTERISTICS OF INFECTION IN THE SNAIL LYMNAEA TRUNCATULA RONDELAUD D amp DREYFUSS G Summary Investigations were carried out in Lymnaea truncatula to determine whether redial burden and shedding of F hepatica cercariae vary when the same population of Lymnaea truncatula is exposed to miracidia that hatched from eggs collected in different naturally infected definitive hosts cattle sheep and rabbits originating from the same region Snails measuring 4 mm in height were each exposed to two miracidia hatched from these eggs and were then raised at 20 C for 30 days The prevalence of infected snails was 35 66 and 86 in the groups exposed to miracidia originating from rabbits sheep and cattle respectively Cercariae were shed from snails of the three groups however shedding varied greatly depending on the origin of the miracidia The total number of cercariae was significantly decreased in the group infected with miracidia from rabbits than in the others 54 5 per snail vs 157 8 and 216 4 The circadian rhythm in the shedding of cercariae was also changed in the former group with maximal shedding between 4 a m and 8 a m No significant difference was noted in the other characteristics of snail infection between the three groups Histological examination of infected snails revea led th
7. at the total number of rediae was significantly decreased at day 30 in the snails infected from miracidia that originated from rabbits than in the other groups a mean of 21 3 vs 38 4 and 43 7 Degenerated free rediae were most numerous in the for mer group than in the two others The definitive host species may play a role in the development of Fasciola infection in the snail by limiting redial and cercarial burdens From this study trematode eggs collected in cattle or sheep are more efficient for transmission of the disease than those obtained from rabbits KEY WORDS cercaria definitive host Fasciola hepatica Lymnaea trunca tula parasite productivity redia INTRODUCTION asciolosis is an economically important disease caused by Fasciola hepatica in temperate regions and its occurrence is dependent on the presence of Lymnaea truncatula populations for the development of parthenitae This trematode can affect a wide range of susceptible hosts including sheep cattle and also wild mammals such as rabbits Haroun and Hillyer 1986 Facult de M decine Laboratoire d Histopathologie Parasitaire and Facult de Pharmacie Laboratoire de Parasitologie 2 rue du Docteur Raymond Marcland F 87025 Limoges Cedex France Correspondence Dr D Rondelaud Facult de M decine F 87025 Limoges Cedex Tel 55 43 58 33 Fax 55 43 58 01 PRET R sum FASCIOLA HEPATICA L INFLUENCE DE L H TE D FINITIF
8. of experiment MATERIALS AND METHODS SNAILS AND PARASITE he population of L truncatula was living in a swampy meadow at Le Treuil Commune of Limoges Landouge Department of Haute Vienne France This colony was known to be devoid of any trematode infection because of regular sampling at the site and histological examination in 70 of the snails collected A total of 600 snails height 4 0 1 mm were collected in this meadow They were transported to the laboratory in isothermal conditions and acclimatized for at least 48 hours in standard aquaria before being subjected to the expe riment The eggs of F hepatica were collected at the slaugh terhouse of Limoges France from gallbladders of naturally infected cattle or sheep whose liver was dis trained for distomatosis The two oxen originated from a herd which was living in a first farm in the Commune of Nieul Department of Haute Vienne and the three sheep came from another farm located in the same valley near the first farm A total of seven wild rabbits Oryctolagus cuniculus were killed by hunters in this valley and contained two to five adult parasites in their liver Eggs were also col lected from gallbladders within two hours after the death of the rabbits All eggs were incubated for 20 days at 20 C in total darkness according to the method described by Ollerenshaw 1971 EXPERIMENTAL PROTOCOL Three groups of 200 snails each were constituted The snail
9. oliasis A review Veterinary Parasitology 1986 20 63 93 MOUAHID A amp THERON A Schistosoma bovis variability of cercarial production as related to the snail hosts Bulinus truncatus B wrightiand Planorbarius metidjen sis International Journal for Parasitology 1986 17 1431 1434 OLLERENSHAW C B Some observations on the epidemiology of fascioliasis in relation to the timing of molluscicide applications in the control of the disease Veterinary Record 1971 98 152 164 PAGES J R amp TH RON A Analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium S intercalatum and S bovis and their hybrid progeny International Journal for Parasitology 1990 20 193 197 RONDELAUD D amp BARTHE D Arguments et propositions pour une nouvelle interpr tation de l volution de Fasciola hepatica L dans Lymnaea Galba truncatula M ller Annales de Parasitologie humaine et compar e 1978 53 201 213 RONDELAUD D amp BARTHE D Les g n rations r diennes de Fasciola hepatica L chez Lymnaea truncatula M ller A propos des effets de plusieurs facteurs Annales de Parasitologie humaine et compar e 1982 57 245 262 STAT ITCF 1987 Manuel d utilisation Institut Technique des C r ales et des Fourrages Service des tudes Statistiques Boigneville 210 p Accept le 28 avril 1995
10. posed to miracidia The number of snails with live parthenitae on serial sec tions was respectively 62 55 and 17 whereas in Parasite 1995 2 275 280 infected snails with or without emission it was 84 48 and 21 The overall prevalence of Fasciola infec tion in these groups was also significantly higher p lt 0 01 in snails infected with miracidia of cattle and sheep origins 86 and 66 respectively than in those infected with miracidia of rabbit origin 35 CERCARIAL SHEDDING Table I gives the different results recorded in the infections derived from the three origins of Fasciola eggs The frequency of snails with shedding was 80 9 in the cattle group 64 5 in the sheep group and 47 6 in the rabbit group The onset of the patent period was similar in the three groups from day 45 to day 51 The mean duration of this period ranged from 35 days in the rabbit group to 60 days in the cattle group but the differences in the mean numbers between these three groups were insignifi cant The shell height was also similar in the three groups a mean of 6 to 6 4 mm Cercaria production was significantly higher F 31 2 p lt 0 001 in the cattle and sheep groups than in the rabbit group 216 and 157 respectively per snail instead of 54 The percentage of floating cysts was almost similar in the three groups from 5 1 to 6 4 Shedding waves were more numerous in the cattle and sheep groups 9 and 8 respectively
11. s of the first group were individually expo sed for four hours in 35 mm petri dishes to two F hepatica miracidia that had hatched from eggs collec ted in cattle The same protocol of infection was used in the two other groups but the Fasciola eggs came from sheep or from rabbit The snails were then rai sed in closed circuit aquaria for 30 days at 20 C with five snails per liter of water Half of the water volume calcium content 12 mg l contained in aquaria was changed twice weekly At day 30 the surviving snails of each group were divided in two subgroups The snails from the first subgroup were individually placed in 35 mm diame ter petri dishes with 2 3 ml of water and a piece of lettuce Daily monitoring consisted of counting meta cercariae and changing water until the snail s death The shell height of the dead snails was then measu red The snails from the second subgroup were dip ped at day 30 into Bouin s fixative following by immediate breaking of the shell under the stereomi croscope Serial sections 5 pm thick were cut and stained using Harris hematoxylin modified Gabe s tri chrome stains A special count was performed every hour for three days in infected snails of the first subgroups 10 per group to determine the time of maximal shedding PARAMETERS UTILIZED Snail infection rates were calculated by dividing the number of infected snails by the number of survivors on day 30 The parameters
12. te d finitif peut donc jouer un r le dans le d veloppement de I infestation fasciolienne chez le mol lusque en limitant le nombre des r dies et la production cercarienne Il ressort de cette tude que les ufs du tr matode r colt s chez les bovins ou les ovins sont plus efficaces pour la transmission de la maladie que ceux provenant de lapins MOTS CL S cercaire Fasciola hepatica h te d finitif Lymnaea truncatula productivit parasitaire r die Little data are currently available on the bionomics of Fasciola infection in L truncatula when the same colony of snails is exposed to different strains of F hepatica miracidia Differences in infection rate and cercaria production were reported by Boray 1966 1969 in the same population of L truncatula expo sed to miracidia from different geographical origins Because of this last finding the following questions arose what is the success of intermediate host infec tion when different origins of F hepatica are tested and consequently what is the best origin of trema tode eggs for transmission of the disease To answer these questions we subjected the same population of L truncatula to miracidia that originated from eggs collected in cattle sheep or wild rabbit gallbladders 275 276 Investigations were carried out in two ways a the cercaria production of F hepatica from these snails and b the histological examination of the redial bur den at day 30
13. ted free rediae B dependent rediae C live free rediae 278 a ES E 0 01 but the difference between the sheep and the cattle groups was not significant Live rediae were diversely affected No significant dif ferences in the mean numbers between the three groups were noted for dependent rediae 4 9 to 7 3 per snail On the other hand the number of free rediae was 3 7 in the rabbit group instead of 22 7 in the sheep group and 29 8 in the cattle group Comparison of the mean values revealed a significant difference only between the rabbit group and the two others F 21 47 p lt 0 001 Mature rediae represented 44 to 52 of live free rediae at day 30 in the cattle and sheep groups In the rabbit group all these latter rediae were mature at this date data not shown DISCUSSION rom our results the characteristics of Fasciola infection in the same population of L trunca tula vary when the miracidia originate from eggs collected from different definitive hosts These modifications principally involved snails that were exposed to miracidia that originated from eggs collec ted in rabbits These findings indicate that the defini tive host species plays a role in the development of Fasciola infection in the snail by limiting the number of rediae and the cercaria production From these results it shoud also be noted that Fasciola eggs col lected in cattle and sheep are more efficient for trans mission of
14. the disease than those obtained from rabbit Problems of compatibility between snail strain and F hepatica have already been studied by Boray 1969 1978 who showed that prevalence and cercaria pro duction can be modified according to the strain s ori gin Some variation in the prevalence of F hepatica 41 to 51 at day 30 of experiment and the total number of rediae 18 to 22 per snail has also been noted by Rondelaud and Barthe 1982 in the same colony of L truncatula exposed to different strains of miracidia that originated from cattle from three geo graphical origins These results demonstrate that the definitive host plays a greater than previously believed role in the development of Fasciola parthenitae in the snail Hillyer and Haroun 1986 demonstrated in their review that the development of adult trematode in the definitive host varies in relation with the mamma lian species and in this context it is logical to assume that the trematode eggs were directly affected by the developmental conditions of the adult parasite These changes in several rabbit group parameters concord with Euzeby s observations 1971 when he discovered that the hatching rate of F hepatica eggs excreted by rabbits was only 30 whereas it ranged from 60 to 85 from the eggs collected in cattle According to Euzeby 1971 growth of the adult parasite in the rabbit is impaired diminishing egg fer tility This hypothesis provides an e
15. xplanation for the reduction in Fasciola prevalence and the number of rediae and cercariae in the rabbit group On the other hand two results warrant particular comments First the significant increase recorded in the number of degenerated free rediae in the rabbit group is difficult to interpret in the light of our cur rent knowledge on the L truncatula F hepatica model If the developmental pattern of F hepatica rediae proposed by Rondelaud and Barthe 1978 1982 is accepted it is logical to assume that the development of Fasciola parthenitae in the snail body would be inhibited by the host during the first two weeks after exposure and that this inhibition would diminish and even disappear in subsequent weeks This process would be enhanced in parthenitae that hatched from eggs collected in rabbits as compared with those which originated from eggs collected in cattle and sheep This hypothesis is based on the numbers of degenerated rediae and those of depen dent rediae found in the three groups Second the results pertaining to the circadian rhythm in cercarial sheddings found in the cattle and sheep groups concord with data reported by Audousset et al 1989 in L truncatula where maximal shedding occurred between midnight and 1 a m On the other hand it is more difficult to explain why maximal sheddings were recorded between 4 and 8 a m in the rabbit group The changes in circadian rhythm repor ted by Mouahid and Th ron 1
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