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Calicophoron daubneyi infection in grazing goats: Results from a cross-sectional coprological survey in France
Small Ruminant Research 82 (2009) 66–68
Contents lists available at ScienceDirect
Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Short communication
Calicophoron daubneyi infection in grazing goats: Results from a cross-sectional coprological survey in France C. Paraud a,∗ , E. Fournier b , V. Robergeot b , A. Kulo c , I. Pors a , C. Baudry a , C. Chartier a a b c
French Food Safety Agency (AFSSA), Laboratoire d’Etudes et de Recherches Caprines, 60 rue de Pied de Fond, 79012 Niort Cedex, France Groupement départemental de défense sanitaire 71 (GDDS 71), 99 rue des Grands Crus, Loché, 71000 Macon, France Ecole Supérieure d’Agronomie, Université de Lomé, BP 1515, Lome, Togo
a r t i c l e
i n f o
Article history: Received 22 November 2007 Received in revised form 8 January 2009 Accepted 12 January 2009 Available online 14 February 2009 Keywords: Calicophoron daubneyi Goat Epidemiology France
a b s t r a c t Infection of grazing goats by Calicophoron daubneyi has already been described in France, in particular in the Saône-et-Loire area (eastern France). The aim of the present study was to describe more precisely the distribution of this parasite in this area. Forty-two goat farms using pasture were visited once at the end of 2006: 15 goats per farm were individually sampled for faeces and the farmer filled in a questionnaire on general characteristics of the farm, on the use of pasture and on the management of parasitism. C. daubneyi infection was equally present in the whole area. 58.1% of the farms presented at least one animal excreting C. daubneyi eggs. Intra-flock prevalence was on average 35% and varied from 7% to 93%. 72.5% of the positive goats excreted less than 100 eggs/g. 70% of the farmers treating their goats for trematode infections used oxyclozanide with two main doses, 15 and 22 mg/kg bodyweight (BW). © 2009 Elsevier B.V. All rights reserved.
1. Introduction Calicophoron daubneyi is a rumen fluke, previously named Paramphistomum daubneyi (Eduardo, 1983). In Europe, this infection has been described in cattle (France, Spain) (Szmidt-Adjidé et al., 2000; Díaz et al., 2007) and in sheep (Italy) (Cringoli et al., 2004). In Europe, the medical and economic importance of this infection is usually considered as low. However, the immature stages of Paramphistomidae can cause severe pathology (diarrhoea and anorexia) and even kill the hosts in heavy infections, as described by Horak (1971) or in French cattle by Dorchies et al. (2002). Two surveys have reported the presence of paramphistomes in French dairy goats. Silvestre et al. (2000) described it for the first time by slaughtering goats originating from Quercy (southern France). These authors recorded a prevalence of 11.5%. By the same type of sur-
∗ Corresponding author. Tel.: +33 5 49 79 61 28; fax: +33 5 49 79 42 19. E-mail address: [email protected] (C. Paraud). 0921-4488/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2009.01.009
vey but with goats coming from Saône-et-Loire (eastern France), Doumenc (2003) reported a prevalence of paramphistome infection of 58.7%. This author identified the species infecting goats in this area as C. daubneyi. Data on infection with paramphistome infection in the French goat flock are scarce and the epidemiology of infection is not well-known. The purpose of the present study was to describe precisely the distribution of paramphistome in grazing goats in the Saône-et-Loire area by a coprological study. 2. Materials and methods The target population consisted of the dairy-goat farms of Saône-etLoire, having more than 10 goats and using pasture (351 farms). Among these, 42 farms were randomly chosen. All the selected farms were located in the western part of the department where are concentrated goat flocks often associated with beef cattle herds. No anthelmintic treatment has been applied during the last 2 months in these farms. From mid-November to mid-December 2006, individual faecal samples were collected per rectum from 15 animals randomly chosen in each farm. On two farms, the whole flock comprised less than 15 goats, so all the goats present were sampled. Age and identification number were recorded
C. Paraud et al. / Small Ruminant Research 82 (2009) 66–68
67
for each animal. In addition, the farmers filled in a questionnaire in order to collect general data on characteristics of the farm as well as on grazing and parasite management. Individual faecal egg counts were performed using a modified McMaster method with potassium iodomercurate solution (d = 1.44), with an additional flotation slide where each egg counted represented 7 eggs per gram of faeces (epg) (Raynaud, 1970). Eggs of C. daubneyi, Dicrocoelium lanceolatum and gastrointestinal strongyles were enumerated. The presence of Fasciola hepatica and Moniezia sp. eggs and of Muellerius capillaris larvae were only recorded. Correlations between age and individual faecal egg excretion of C. daubneyi and between flock prevalence and mean flock egg excretion was analyzed by a Spearman non-parametrical correlation at a level p < 0.05. The statistical analyses were performed using Systat 1.9, 1999.
3. Results
Fig. 1. Mean faecal egg excretion (epg) according to the intra-flock prevalence (%).
3.1. Flocks characteristics, pasture management, animals The sampled flocks comprised between 12 and 147 goats (mean: 68 goats). 86% of the farmers (95% confidence interval: 76–96%) were cheese-makers. The usual grazing period was from March to November. Twenty-three farmers (54%, 95% CI: 38–69%) used three paddocks or less, comprising mainly permanent pastures. In 21 farms (50%, 95% CI: 35–65%), the goats had free access to water (marshes, ponds or springs) on pasture. Thirty-one owners (74%, 95% CI: 61–87%) reared simultaneously goats and cattle and practiced mixed or alternate grazing with the two species. Six hundred and nine goats were individually sampled. The percentage of goats sampled per flock varied from 10 to 100%, with a mean of 32.8% (95% CI: 26.3–39.2%). Mean age of the sampled goats was 4.2 (range: 1–12). 3.2. Calicophoron daubneyi infection C. daubneyi infection was equally present in the department. Twenty-four farms (57%, 95% CI: 42–72%) had at least one positive goat for C. daubneyi. Apparent intra-flock prevalence was on average 35% and varied from 7% to 93%. Co-infection by C. daubneyi–F. hepatica was found in two farms. With respect to animals, 115 goats (19%, 95% CI: 16–22) were positive with an average egg output of 157 epg (range: 7–5950). 67 of them (58%, 95% CI: 49–67) excreted less than 50 epg. Age was not significantly correlated to the faecal excretion of C. daubneyi eggs (p = 0.126). Correlation between intra-flock prevalence and mean flock faecal egg counts was significant and positive (p < 0.001) (Fig. 1). Thirty-four farmers (81%, 95% CI: 68–92) applied treatments to control trematode infections, usually once a year during the dry period. 70% (24 farmers) of them used oxyclozanide with two main doses: 15 mg/kg bodyweight (BW) or 22 mg/kg BW once per oral route. 3.3. Other helminth infection Nearly all the flocks were infected by gastrointestinal strongyles. 481 goats had positive faecal egg counts for
strongyles (79%, 95% CI: 76–82) with a mean faecal egg count of 960 epg (range: 7–9900). Thirty-six farms (62%, 95% CI: 47–77) were infected by D. lanceolatum. Seventy-seven goats excreted eggs in faeces with an average intensity of 73 epg (range: 7–250). On the contrary, F. hepatica infection was scarce: only three goats belonging to three different farms were found positive for this infection. Co-infection by the two liver flukes was found in one farm. 4. Discussion/conclusion This study confirms the high prevalence of paramphistome infection in Saône-et-Loire yet reported by Doumenc (2003). The coprological prevalence recorded in our study (19.2%) is lower than the coprological prevalence observed by this author (41.3%). In the same way, individual mean faecal egg excretion was 157 epg with most of the goats excreting less than 50 epg while Doumenc (2003) reported a mean faecal egg count of 318 epg. These differences may be due to the type of goats involved: Doumenc (2003) used culled dairy goats, probably older and in poorer condition than the lactating goats involved in the present study. Data about usual intra-flock prevalence are lacking for goats but exist for cattle and for sheep. Abrous et al. (1999) reported prevalences of C. daubneyi infection in farms from central France varying from 2.7% to 86.3% for cattle and from 16.0 to 75.0% for sheep, which is similar to the intra-flock prevalences reported here. A significant positive correlation was observed between the flock prevalence and the mean faecal egg excretion. To our knowledge, this is the first time that such a relationship is demonstrated. Results on the relationship between age and paramphistome faecal egg excretion are conflicting. Our findings are in agreement with the results of Szmidt-Adjidé et al. (2000). These authors, using a slaughterhouse study, did not demonstrate any correlation between paramphistome infection and age in cattle. On the contrary, Dorchies et al. (1998) reported that the older cows were the most infected and this was confirmed by González-Warleta et al. (2008). The absence of relationship between age and paramphistome faecal egg excretions may be due to the high percentage of owners carrying out routine annual treatment with oxyclozanide.
68
C. Paraud et al. / Small Ruminant Research 82 (2009) 66–68
Several factors influence the environmental contamination with paramphistome metacercariae. First, climatic and topographical characteristics influence the intermediate host populations and affect the prevalence of ruminant paramphistome infection (Cringoli et al., 2004; Díaz et al., 2007). Secondly, Horak (1971) suggested that cattle can play a role as source of infection for sheep via the contamination of the environment. In this study, the low variability of climatic characteristics in the studied area and of grazing practices between the farms did not permit the demonstration of the existence of such risk factors in this region. Silvestre et al. (2000) tested the effect of 2 putative risk factors (presence of water on pastures, mixed grazing with cattle) on paramphistome infection prevalence in the 22 goat farms they surveyed and they were unable to correlate these factors with the presence of infection. Finally, this study points out that in this area, the main anthelmintic used to control paramphistome infections is oxyclozanide with two different doses: 15 or 22 mg/kg. Two experiments recorded the efficacy of oxyclozanide on paramphistomes in goats. Sahai et al. (1983) obtained 100% of reduction of the parasite burdens of Paramphistomum cervi after administration of oxyclozanide at the dose of 15 mg/kg BW to experimentally infected kids. Paraud et al. (2008) reported reductions of the worm burdens by more than 95% with doses of oxyclozanide of 15 and 22.5 mg/kg BW in goats experimentally infected by C. daubneyi. The therapeutic schemes recorded in the present study seem efficient, with the limit that French regulations impose a maximal volume of administration named “Stop-dose” which is equal to 20 ml of the 3.4% solution for all the animals weighing more than 45 kg. This regulation is followed by most of the farmers, which may lead to under-dosage in the heaviest goats. Acknowledgement We thank all the farmers who have participated in this survey.
References Abrous, M., Rondelaud, D., Dreyfuss, G., Cabaret, J., 1999. Infection of Lymnea truncatula and Lymnea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France. Vet. Res. 30, 113–118. Cringoli, G., Taddei, R., Rinaldi, L., Veneziano, V., Musella, V., Cascone, C., Sibilio, G., Malone, J.B., 2004. Use of remote sensing and geographical information systems to identify environmental features that influence the distribution of paramphistomosis in sheep from the southern Italian Apennines. Vet. Parasitol. 122, 15–26. Díaz, P., Paz-Silva, A., Sánchez-Andrade, R., Suárez, J.L., Pedreira, J., Arias, ˜ M., Díez-Banos, P., Morrondo, P., 2007. Assessment of climatic and orographic conditions on the infection by Calicophoron daubneyi and Dicrocoelium dendriticum in grazing beef cattle (NW Spain). Vet. Parasitol. 149, 285–289. Dorchies, P., Bergeaud, J.P., Duranton, C., Prévot, F., Tessier, P., 1998. Extension de la paramphistomose bovine en France: résultats d’une enquête coproscopique sur 465 bovins dans treize départements. Rev. Med. Vet. 149 (11), 1029–1032. Dorchies, P., Lacroux, C., Navetat, H., Rizet, C., Guéneau, E., Bisson, B., Ferté, H., 2002. Trois cas d’une nouvelle entité pathologique: la paramphistomose larvaire chez les bovins. Bulletin des Groupements Techniques Vétérinaires 13, 91–93. Doumenc, V., 2003. Helminthofaune des caprins en Saône-et-Loire: influence du pâturage mixte avec les bovins. Thesis, Doctorate in Veterinary Medicine, Toulouse (France), n◦ 4047, 100 pp. Eduardo, S.L., 1983. The taxonomy of the family Paramphistomidae Fischoeder, 1901 with special reference of the morphology of species occurring in ruminants. III. Revision of the genus Calicophoron Nasmark, 1937. Syst. Parasitol. 5, 25–79. González-Warleta, M., García-Presedo, I., Castro-Hermida, J.A., ˜ Minambres, B., González-Lanza, C., Mezo, M., Manga-González, Y., 2008. Cattle slaughterhouse and field studies on the Calicophoron daubneyi (Dinnik 1962; Eduardo, 1983) infection (NW Spain). In: Xth European Multicolloquium of Parasitology, Paris, 24–29 August 2008. Horak, I.G., 1971. Paramphistomiasis of domestic animals. Adv. Parasitol. 9, 33–72. Paraud, C., Gaudin, C., Pors, I., Chartier, C., 2008. Efficacy of oxyclozanide against the rumen fluke Calicophoron daubneyi in experimentally infected goats. Vet. J., doi:10.1016/j.tvjl.2008.01.002. Raynaud, J.P., 1970. Etude de l’efficacité d’une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Ann. Parasitol. Hum. Comp. 45, 321–342. Sahai, B.N., Ansari, M.Z., Singh, R.P., Prasad, K.D., 1983. Anthelmintic efficacy of terenol and zanil against experimental paramphistomiasis in goats. Indian J. Vet. Med. 3 (1), 27–32. Silvestre, A., Sauvé, C., Cabaret, J., 2000. Caprine Paramphistomum daubneyi (Trematoda) infection in Europe. Vet. Rec. 146, 674–675. Szmidt-Adjidé, V., Abrous, M., Adjidé, C.C., Dreyfuss, G., Lecompte, A., Cabaret, J., Rondelaud, D., 2000. Prevalence of Paramphistomum daubneyi infection in cattle in central France. Vet. Parasitol. 87, 133–138.
Contents lists available at ScienceDirect
Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Short communication
Calicophoron daubneyi infection in grazing goats: Results from a cross-sectional coprological survey in France C. Paraud a,∗ , E. Fournier b , V. Robergeot b , A. Kulo c , I. Pors a , C. Baudry a , C. Chartier a a b c
French Food Safety Agency (AFSSA), Laboratoire d’Etudes et de Recherches Caprines, 60 rue de Pied de Fond, 79012 Niort Cedex, France Groupement départemental de défense sanitaire 71 (GDDS 71), 99 rue des Grands Crus, Loché, 71000 Macon, France Ecole Supérieure d’Agronomie, Université de Lomé, BP 1515, Lome, Togo
a r t i c l e
i n f o
Article history: Received 22 November 2007 Received in revised form 8 January 2009 Accepted 12 January 2009 Available online 14 February 2009 Keywords: Calicophoron daubneyi Goat Epidemiology France
a b s t r a c t Infection of grazing goats by Calicophoron daubneyi has already been described in France, in particular in the Saône-et-Loire area (eastern France). The aim of the present study was to describe more precisely the distribution of this parasite in this area. Forty-two goat farms using pasture were visited once at the end of 2006: 15 goats per farm were individually sampled for faeces and the farmer filled in a questionnaire on general characteristics of the farm, on the use of pasture and on the management of parasitism. C. daubneyi infection was equally present in the whole area. 58.1% of the farms presented at least one animal excreting C. daubneyi eggs. Intra-flock prevalence was on average 35% and varied from 7% to 93%. 72.5% of the positive goats excreted less than 100 eggs/g. 70% of the farmers treating their goats for trematode infections used oxyclozanide with two main doses, 15 and 22 mg/kg bodyweight (BW). © 2009 Elsevier B.V. All rights reserved.
1. Introduction Calicophoron daubneyi is a rumen fluke, previously named Paramphistomum daubneyi (Eduardo, 1983). In Europe, this infection has been described in cattle (France, Spain) (Szmidt-Adjidé et al., 2000; Díaz et al., 2007) and in sheep (Italy) (Cringoli et al., 2004). In Europe, the medical and economic importance of this infection is usually considered as low. However, the immature stages of Paramphistomidae can cause severe pathology (diarrhoea and anorexia) and even kill the hosts in heavy infections, as described by Horak (1971) or in French cattle by Dorchies et al. (2002). Two surveys have reported the presence of paramphistomes in French dairy goats. Silvestre et al. (2000) described it for the first time by slaughtering goats originating from Quercy (southern France). These authors recorded a prevalence of 11.5%. By the same type of sur-
∗ Corresponding author. Tel.: +33 5 49 79 61 28; fax: +33 5 49 79 42 19. E-mail address: [email protected] (C. Paraud). 0921-4488/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2009.01.009
vey but with goats coming from Saône-et-Loire (eastern France), Doumenc (2003) reported a prevalence of paramphistome infection of 58.7%. This author identified the species infecting goats in this area as C. daubneyi. Data on infection with paramphistome infection in the French goat flock are scarce and the epidemiology of infection is not well-known. The purpose of the present study was to describe precisely the distribution of paramphistome in grazing goats in the Saône-et-Loire area by a coprological study. 2. Materials and methods The target population consisted of the dairy-goat farms of Saône-etLoire, having more than 10 goats and using pasture (351 farms). Among these, 42 farms were randomly chosen. All the selected farms were located in the western part of the department where are concentrated goat flocks often associated with beef cattle herds. No anthelmintic treatment has been applied during the last 2 months in these farms. From mid-November to mid-December 2006, individual faecal samples were collected per rectum from 15 animals randomly chosen in each farm. On two farms, the whole flock comprised less than 15 goats, so all the goats present were sampled. Age and identification number were recorded
C. Paraud et al. / Small Ruminant Research 82 (2009) 66–68
67
for each animal. In addition, the farmers filled in a questionnaire in order to collect general data on characteristics of the farm as well as on grazing and parasite management. Individual faecal egg counts were performed using a modified McMaster method with potassium iodomercurate solution (d = 1.44), with an additional flotation slide where each egg counted represented 7 eggs per gram of faeces (epg) (Raynaud, 1970). Eggs of C. daubneyi, Dicrocoelium lanceolatum and gastrointestinal strongyles were enumerated. The presence of Fasciola hepatica and Moniezia sp. eggs and of Muellerius capillaris larvae were only recorded. Correlations between age and individual faecal egg excretion of C. daubneyi and between flock prevalence and mean flock egg excretion was analyzed by a Spearman non-parametrical correlation at a level p < 0.05. The statistical analyses were performed using Systat 1.9, 1999.
3. Results
Fig. 1. Mean faecal egg excretion (epg) according to the intra-flock prevalence (%).
3.1. Flocks characteristics, pasture management, animals The sampled flocks comprised between 12 and 147 goats (mean: 68 goats). 86% of the farmers (95% confidence interval: 76–96%) were cheese-makers. The usual grazing period was from March to November. Twenty-three farmers (54%, 95% CI: 38–69%) used three paddocks or less, comprising mainly permanent pastures. In 21 farms (50%, 95% CI: 35–65%), the goats had free access to water (marshes, ponds or springs) on pasture. Thirty-one owners (74%, 95% CI: 61–87%) reared simultaneously goats and cattle and practiced mixed or alternate grazing with the two species. Six hundred and nine goats were individually sampled. The percentage of goats sampled per flock varied from 10 to 100%, with a mean of 32.8% (95% CI: 26.3–39.2%). Mean age of the sampled goats was 4.2 (range: 1–12). 3.2. Calicophoron daubneyi infection C. daubneyi infection was equally present in the department. Twenty-four farms (57%, 95% CI: 42–72%) had at least one positive goat for C. daubneyi. Apparent intra-flock prevalence was on average 35% and varied from 7% to 93%. Co-infection by C. daubneyi–F. hepatica was found in two farms. With respect to animals, 115 goats (19%, 95% CI: 16–22) were positive with an average egg output of 157 epg (range: 7–5950). 67 of them (58%, 95% CI: 49–67) excreted less than 50 epg. Age was not significantly correlated to the faecal excretion of C. daubneyi eggs (p = 0.126). Correlation between intra-flock prevalence and mean flock faecal egg counts was significant and positive (p < 0.001) (Fig. 1). Thirty-four farmers (81%, 95% CI: 68–92) applied treatments to control trematode infections, usually once a year during the dry period. 70% (24 farmers) of them used oxyclozanide with two main doses: 15 mg/kg bodyweight (BW) or 22 mg/kg BW once per oral route. 3.3. Other helminth infection Nearly all the flocks were infected by gastrointestinal strongyles. 481 goats had positive faecal egg counts for
strongyles (79%, 95% CI: 76–82) with a mean faecal egg count of 960 epg (range: 7–9900). Thirty-six farms (62%, 95% CI: 47–77) were infected by D. lanceolatum. Seventy-seven goats excreted eggs in faeces with an average intensity of 73 epg (range: 7–250). On the contrary, F. hepatica infection was scarce: only three goats belonging to three different farms were found positive for this infection. Co-infection by the two liver flukes was found in one farm. 4. Discussion/conclusion This study confirms the high prevalence of paramphistome infection in Saône-et-Loire yet reported by Doumenc (2003). The coprological prevalence recorded in our study (19.2%) is lower than the coprological prevalence observed by this author (41.3%). In the same way, individual mean faecal egg excretion was 157 epg with most of the goats excreting less than 50 epg while Doumenc (2003) reported a mean faecal egg count of 318 epg. These differences may be due to the type of goats involved: Doumenc (2003) used culled dairy goats, probably older and in poorer condition than the lactating goats involved in the present study. Data about usual intra-flock prevalence are lacking for goats but exist for cattle and for sheep. Abrous et al. (1999) reported prevalences of C. daubneyi infection in farms from central France varying from 2.7% to 86.3% for cattle and from 16.0 to 75.0% for sheep, which is similar to the intra-flock prevalences reported here. A significant positive correlation was observed between the flock prevalence and the mean faecal egg excretion. To our knowledge, this is the first time that such a relationship is demonstrated. Results on the relationship between age and paramphistome faecal egg excretion are conflicting. Our findings are in agreement with the results of Szmidt-Adjidé et al. (2000). These authors, using a slaughterhouse study, did not demonstrate any correlation between paramphistome infection and age in cattle. On the contrary, Dorchies et al. (1998) reported that the older cows were the most infected and this was confirmed by González-Warleta et al. (2008). The absence of relationship between age and paramphistome faecal egg excretions may be due to the high percentage of owners carrying out routine annual treatment with oxyclozanide.
68
C. Paraud et al. / Small Ruminant Research 82 (2009) 66–68
Several factors influence the environmental contamination with paramphistome metacercariae. First, climatic and topographical characteristics influence the intermediate host populations and affect the prevalence of ruminant paramphistome infection (Cringoli et al., 2004; Díaz et al., 2007). Secondly, Horak (1971) suggested that cattle can play a role as source of infection for sheep via the contamination of the environment. In this study, the low variability of climatic characteristics in the studied area and of grazing practices between the farms did not permit the demonstration of the existence of such risk factors in this region. Silvestre et al. (2000) tested the effect of 2 putative risk factors (presence of water on pastures, mixed grazing with cattle) on paramphistome infection prevalence in the 22 goat farms they surveyed and they were unable to correlate these factors with the presence of infection. Finally, this study points out that in this area, the main anthelmintic used to control paramphistome infections is oxyclozanide with two different doses: 15 or 22 mg/kg. Two experiments recorded the efficacy of oxyclozanide on paramphistomes in goats. Sahai et al. (1983) obtained 100% of reduction of the parasite burdens of Paramphistomum cervi after administration of oxyclozanide at the dose of 15 mg/kg BW to experimentally infected kids. Paraud et al. (2008) reported reductions of the worm burdens by more than 95% with doses of oxyclozanide of 15 and 22.5 mg/kg BW in goats experimentally infected by C. daubneyi. The therapeutic schemes recorded in the present study seem efficient, with the limit that French regulations impose a maximal volume of administration named “Stop-dose” which is equal to 20 ml of the 3.4% solution for all the animals weighing more than 45 kg. This regulation is followed by most of the farmers, which may lead to under-dosage in the heaviest goats. Acknowledgement We thank all the farmers who have participated in this survey.
References Abrous, M., Rondelaud, D., Dreyfuss, G., Cabaret, J., 1999. Infection of Lymnea truncatula and Lymnea glabra by Fasciola hepatica and Paramphistomum daubneyi in farms of central France. Vet. Res. 30, 113–118. Cringoli, G., Taddei, R., Rinaldi, L., Veneziano, V., Musella, V., Cascone, C., Sibilio, G., Malone, J.B., 2004. Use of remote sensing and geographical information systems to identify environmental features that influence the distribution of paramphistomosis in sheep from the southern Italian Apennines. Vet. Parasitol. 122, 15–26. Díaz, P., Paz-Silva, A., Sánchez-Andrade, R., Suárez, J.L., Pedreira, J., Arias, ˜ M., Díez-Banos, P., Morrondo, P., 2007. Assessment of climatic and orographic conditions on the infection by Calicophoron daubneyi and Dicrocoelium dendriticum in grazing beef cattle (NW Spain). Vet. Parasitol. 149, 285–289. Dorchies, P., Bergeaud, J.P., Duranton, C., Prévot, F., Tessier, P., 1998. Extension de la paramphistomose bovine en France: résultats d’une enquête coproscopique sur 465 bovins dans treize départements. Rev. Med. Vet. 149 (11), 1029–1032. Dorchies, P., Lacroux, C., Navetat, H., Rizet, C., Guéneau, E., Bisson, B., Ferté, H., 2002. Trois cas d’une nouvelle entité pathologique: la paramphistomose larvaire chez les bovins. Bulletin des Groupements Techniques Vétérinaires 13, 91–93. Doumenc, V., 2003. Helminthofaune des caprins en Saône-et-Loire: influence du pâturage mixte avec les bovins. Thesis, Doctorate in Veterinary Medicine, Toulouse (France), n◦ 4047, 100 pp. Eduardo, S.L., 1983. The taxonomy of the family Paramphistomidae Fischoeder, 1901 with special reference of the morphology of species occurring in ruminants. III. Revision of the genus Calicophoron Nasmark, 1937. Syst. Parasitol. 5, 25–79. González-Warleta, M., García-Presedo, I., Castro-Hermida, J.A., ˜ Minambres, B., González-Lanza, C., Mezo, M., Manga-González, Y., 2008. Cattle slaughterhouse and field studies on the Calicophoron daubneyi (Dinnik 1962; Eduardo, 1983) infection (NW Spain). In: Xth European Multicolloquium of Parasitology, Paris, 24–29 August 2008. Horak, I.G., 1971. Paramphistomiasis of domestic animals. Adv. Parasitol. 9, 33–72. Paraud, C., Gaudin, C., Pors, I., Chartier, C., 2008. Efficacy of oxyclozanide against the rumen fluke Calicophoron daubneyi in experimentally infected goats. Vet. J., doi:10.1016/j.tvjl.2008.01.002. Raynaud, J.P., 1970. Etude de l’efficacité d’une technique de coproscopie quantitative pour le diagnostic de routine et le contrôle des infestations parasitaires des bovins, ovins, équins et porcins. Ann. Parasitol. Hum. Comp. 45, 321–342. Sahai, B.N., Ansari, M.Z., Singh, R.P., Prasad, K.D., 1983. Anthelmintic efficacy of terenol and zanil against experimental paramphistomiasis in goats. Indian J. Vet. Med. 3 (1), 27–32. Silvestre, A., Sauvé, C., Cabaret, J., 2000. Caprine Paramphistomum daubneyi (Trematoda) infection in Europe. Vet. Rec. 146, 674–675. Szmidt-Adjidé, V., Abrous, M., Adjidé, C.C., Dreyfuss, G., Lecompte, A., Cabaret, J., Rondelaud, D., 2000. Prevalence of Paramphistomum daubneyi infection in cattle in central France. Vet. Parasitol. 87, 133–138.