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Prevalence of Paramphistomum daubneyi infection in cattle in central France
Veterinary Parasitology 87 (2000) 133–138
Prevalence of Paramphistomum daubneyi infection in cattle in central France V. Szmidt-Adjidéa,1 , M. Abrous a , C.C. Adjidé b , G. Dreyfuss a , A. Lecompte c , J. Cabaret d , D. Rondelaud e,∗ a
Laboratoire de Parasitologie, Faculté de Pharmacie, 2, rue du Docteur Raymond Marcland, 87025 Limoges Cedex, France b Service de Bactériologie-Parasitologie-Virologie, Centre Hospitalier Universitaire, B.P. 465, 97159 Pointe-à-Pitre Cedex, Guadeloupe/F.W.I. c Services Vétérinaires, Abattoir Municipal de Limoges, 125, rue de Nexon, 87000 Limoges Cedex, France d Laboratoire de Parasitologie, Institut National de la Recherche Agronomique, 37380 Nouzilly Cedex, France e Laboratoire d’Histopathologie Parasitaire, Faculté de Médecine, 2, rue du Docteur Raymond Marcland, 87025 Limoges Cedex, France Received 12 January 1999; accepted 14 July 1999
Abstract Investigations at the slaughterhouse of Limoges (Central France) were performed in 1994–1996 to determine the prevalence of Paramphistomum daubneyi infection in cattle. In 1994/1995, higher prevalences of P. daubneyi were recorded in May, October, and January. In 1996, smaller variations were recorded, and prevalence in April and May was higher. The prevalence of P. daubneyi in summer was lower. Breed and age of cattle were not significantly associated to P. daubneyi infection, but females were significantly more infected than males. P. daubneyi infection was related to that of Fasciola hepatica, but not to that of Dicrocoelium lanceolatum. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Cattle-Trematoda; Epidemiology; Paramphistomum daubneyi
1. Introduction Paramphistomes may decrease production in cattle (Spence et al., 1996) and also cause disease (Agosti et al., 1980). Their prevalence has been assessed in most European coun∗
Corresponding author. Present address: Service de Biochimie, Centre Hospitalier Universitaire, B.P. 465, 97159 Pointe-`a-Pitre Cedex, Guadeloupe/F.W.I. 1
0304-4017/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 9 9 ) 0 0 1 6 8 - 5
134
V. Szmidt-Adjid´e et al. / Veterinary Parasitology 87 (2000) 133–138
tries. Several studies had been undertaken in France (Graber et al., 1980, and Casset, 1989, in eastern France; Postal, 1984, in western France). According to Levasseur and Alzieu (1991), the following species occur: Paramphistomum cervi, Paramphistomum daubneyi, Paramphistomum ichikawai, and Paramphistomum microbothrium. P. daubneyi seems to be the more frequent species in cattle. Other trematodes are also recorded in these ruminants such as Fasciola hepatica (Mage and Rondelaud, 1983; Recca and Rivière, 1984) and Dicrocoelium lanceolatum, and they might interfere (positively or negatively) with Paramphistomum infections. We were then interested to assess the prevalence of infection by P. daubneyi in Limousin (central France), a region with relatively high prevalence of F. hepatica infection in cattle.
2. Materials and methods A first investigation at the slaughterhouse of Limoges (department of Haute Vienne, France) was organized from February 1994 to January 1995 on a limited number of cattle in order to estimate monthly variations of prevalence. As this parameter showed large variations in winter and spring, a second study was undertaken from January 1996 to June 1996 to appreciate if these variations were due to small sampling or to a real seasonal variation. In the second investigation, cattle recently treated against F. hepatica (with some whitish calcifications on the surface of the liver) were eliminated. The 1994 average monthly temperature ranged from approximately 5◦ C in December, January, and February to 20◦ C in July and August in Limoges. The yearly rainfall was 1440 mm, and ranged from 200 mm in September to 25 mm in July, in 1994. Paramphistomids found in cattle were P. daubneyi. As the adult worms of the genus Paramphistomum necessitated an histological examination of suckers, we have used the gross morphology and chaetotaxy of the cercaria (Szmidt-Adjidé, 1996), and the local species of the lymnaeid snail (Lymnaea truncatula) used as intermediate host (Szmidt-Adjidé et al., 1994) to identify this paramphistome. The prevalence of infection was recorded using the ratio between the number of infected cattle and that of examined cattle. The intensity of infection in the paunch of cattle was classified into: 0, 1–10, 11–100, 101–200, and more than 200 paramphistomes. In the first investigation, P. daubneyi infection only was studied and the characteristics of hosts were not recorded. In the second investigation, cattle breed, age (younger or older than 2 years), and gender were recorded, and infection with the trematodes D. lanceolatum and F. hepatica were noted. Univariate tests (chi-square, likelihood ratio) were performed with a Simstat software (Péladeau and Lacouture, 1993). The infection odds ratio (OR) and Cornfield interval of confidence at 95% were calculated using software Epi-Info (1991). An OR > 1 indicates that the factors are positively associated with infection. A p value less than 5% was considered statistically significant. The calculations and their rationale are explained by Kleinbaum et al. (1982).
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Table 1 P. daubneyi seasonal prevalence and intensity of infection in cattle from the Limousin region Trial
Sampling month
1994–1995
1996
a b
February March April May June July August September October November December January January February March April May June
Number of cattle examined
52 21 25 20 20 20 25 25 25 25 26 26 170 288 299 203 343 128
Prevalence of infection (%)
0.27 0.10 0.16 0.45 0.15 0.10 0.12 0.08 0.40 0.20 0.19 0.46 0.22 0.21 0.24 0.29 0.29 0.22
Intensity of infectiona (%) Pd 1
Pd 2
Pd 3
Pd 4
0.52 0.50 0.25 0 0 0 0.67 0 0.31 0 0 0.44 0.34 0.28 0.50 0.37 0.26 0.25
0.22 0 0 0.33 0.33 0.33 0 0.50 0.21 0.62 0 0.14 0.48 0.41 0.28 0.47 0.38 0.43
0.15 0 0.50 0.22 0.67 0.67 0.33 0.50 0.31 0 0.19 0.28 0.18 0.20 0.24 0.14 0.32 0.30
0.11b 0.50 0.25 0.45 0 0 0 0 0.17 0.38 0.81 0.14 0 0.01 0.01 0.02 0.04 0.02
Pd 1 (1–10 paramphistomes per ruminant), Pd 2 (11–100), Pd 3 (101–200), Pd 4 (more than 200). Percentage of each class among infected cattle.
3. Results 3.1. Seasonal evolution (Table 1) In 1994/1995, higher prevalence values were recorded in May, October, and January (chi-square or likelihood ratio: p < 0.01). In 1996, smaller variations were recorded and higher prevalences, although non significant (chi-square: p = 0.11), in the first 6 months of the year were found in April and May, which was similar to the preceding investigation (May). When each season was considered, P. daubneyi prevalence was 0.11 in Summer (July, August, and September) instead of 0.30 in Winter, 0.38 in Spring, and 0.36 in Autumn. A statistical difference between these seasons was found (chi-square: p < 0.01), indicating that Summer corresponded to lower infection by P. daubneyi. In 1996, significant differences in the intensity of P. daubneyi infection were found in relation with the month of sampling, May corresponding to the highest infections. 3.2. Host at risk (Table 2) Breed and age were not significantly associated to the prevalence of P. daubneyi infection, whereas gender was significantly associated to prevalence (chi-square: p < 0.01). Females were significantly more frequently infected than males (Odds-ratio OR = 2.17, con-
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Table 2 Breed, age, and gender of cattle in relation to the prevalence of trematode infections in the Limousin region, France Breed
Age
Limousine
Less than 2 years
Aquitaine Blonde
More than 2 years Less than 2 years
Frisian a
More than 2 years Less than 2 years More than 2 years
Gender (number of examined cattle)
Female (1016) Male (75) Female (74) Female (68) Male (29) Female (12) Female (114) Female (38)
Prevalence of infectiona P. daubneyi
F. hepatica
D. lanceolatum
0.26 ± 0.03 0.16 ± 0.08 0.23 ± 0.10 0.37 ± 0.12 0.10 ± 0.10 0 0.19 ± 0.37 0.37 ± 0.15
0.07 0.05 0.09 0.09 0 0 0.17 0.05
0.06 0.03 0.05 0.03 0 0 0.01 0.05
Confidence interval at 95%.
fidence interval: 1.20–4.0, p < 0.01). This characteristic was not observed with F. hepatica (OR = 2.29, confidence interval: 0.83–6.33, p = 0.11). No significant differences (chi-squares ranging from 2.2 to 3.3, with significance of p = 0.50–0.30) between the intensities of P. daubneyi infection were recorded in relation to breed, age, gender, or co-infection with other trematodes (data not shown). This means that intensity of infection was not related to any of the factors we studied. 3.3. Trematode associations Prevalence of D. lanceolatum infection was not related to that of P. daubneyi infection. Conversely, prevalences of F. hepatica and of P. daubneyi were correlated (OR = 2.15, confidence interval: 1.44–3.20, p = 0.003).
4. Discussion Prevalence of P. daubneyi infection was on average at 20%, which is much higher than that recorded in one site in France (Casset, 1989; 5.5%), but is similar in another site (Postal, 1984; 14.5%) and to that found in northern Italy (Agosti et al., 1980; 17%) or in Turkey (Tinar et al., 1992; 15%). This might result from actual differences due to different environments, or to an increase in P. daubneyi infection in the last years. Seasonal evolution of infection might be related to climatic variations as shown by Rolfe et al. (1991), depending mostly on rainfall. Rainfall is high in September–October and probably favor cercarial emission in L. truncatula that survived during Summer, which could result into infection of cattle in November–December. Rainfall is also important in January and February, which results into cercaria emission in March and into cattle infection in May. The gender of cattle was the main characteristic that was related to P. daubneyi infection. Females were more infected than males, as already pointed out by Kang and Kim (1988) (68% in females versus 49% in males) or by Asanji (1989). The first explanation concerned
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a longer maintenance of young males in cowshed for a better growth and a faster sale, whereas females rapidly were in pastures, thus leading to higher prevalences. The second point was due to different recruitment of males and females in slaughter houses: females having production or health problems were culled, whereas it was the normal course of production to eliminate males. The positive association between F. hepatica and P. daubneyi is interesting, as Agosti et al. (1980) have already mentioned a co-infection of cattle by these parasites. An argument to explain this parasite association is that both trematodes utilize L. truncatula as an intermediate host. As this snail was living in swampy zones of meadows grazed by cattle, metacercariae of both trematodes were found in the same places and might be ingested together by ruminants. The differences between the prevalence of each trematode infection in cattle might result from the density of metacercariae on grazed grass, or from the specific development of metacercariae in this definitive host.
Acknowledgements The financial help of the Limousin region in the form of a Ph.D. grant to V. Szmidt-Adjidé is gratefully acknowledged.
References Agosti, M., Cavaletti, E., Pozza, O., 1980. Clinica e epizootologia della paramphistomiasi bovina nella Provincia di Milano. Clin. Vet. 103, 284–296. Asanji, M.F., 1989. Paramphistomiasis of cattle in Sierra Leone and seasonal fluctuations in its prevalence. Bull. Anim. Health Prod. Africa 37, 327–331. Casset, I., 1989. Enquête sur la paramphistomose bovine: recherche des parasites en abattoir. Rev. Méd. Vét. 140, 925–927. Epi-Info, 1991. Version 5.01. CDC, Epidemiology Program Office, Atlanta, Georgia, USA. Graber, M., Chauve, C., Fonteneau, M., 1980. Existence en France de Paramphistomum daubneyi Dinnik, 1962. Bull. Acad. Vét. Fr. 53, 265–271. Kang, Y.B., Kim, S.H., 1988. Rumen fluke infections in slaughtered cattle in Korea. Research reports of the rural development administration. Vet. Korean Republic 30, 12–16. Kleinbaum, D.G., Kupper, L.I., Morgenstern, H., 1982. Epidemiologic Research. Van Nostrand Reinhold, New York, 529 p. Levasseur, G., Alzieu, J.P., 1991. La paramphistomose. Bull. Group Tech. Vét. No 404, 153–155. Mage, C., Rondelaud, D., 1983. Réflexions sur la prévention de la fasciolose en France. Dossiers de l’Elevage 5, 25–28. Péladeau, N., Lacouture, Y., 1993. Simstat: boostrap computer simulation and statistical program for IBM personal computer. Behavior Res. Meth. Inst. Comp. 25, 410–413. Postal, J.M., 1984. Les paramphistomoses gastro-duodénales des Ruminants, Vet. Med. Doct. Thesis, Alfort, France, No 164, 125 p. Recca, A., Rivière, F., 1984. Enquête sur la prévalence et la répartition géographique de la fasciolose bovine en France. Bull. Soc. Vét. Prat. 68, 213–242. Rolfe, P.F., Boray, J.C., Nichols, P., Collins, G.H., 1991. Epidemiology of paramphistomosis in cattle. Int. J. Parasitol. 21, 813–819. Spence, S.A., Fraser, G.C., Chang, S., 1996. Response in milk production to the control of gastro-intestinal nematode and paramphistome parasites in dairy cattle. Aust. Vet. J. 74, 456–459.
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Szmidt-Adjidé, V., 1996. Les distomatoses à Paramphistomum daubneyi Dinnik, 1962 et à Fasciola hepatica Linné, 1758 dans la région du Limousin (France). Infestation des bovins et des mollusques hôtes intermédiaires. Pharm. Sci. Doct. Thesis, Limoges No 302B, 141 p. Szmidt-Adjidé, V., Rondelaud, D., Dreyfuss, G., 1994. Premières données sur l’infestation naturelle de Lymnaea truncatula Müller par Paramphistomum daubneyi Dinnik dans le département de la Haute-Vienne. Bull. Soc. Fr. Parasitol. 12, 183–188. Tinar, R., Coskun, S.Z., Dogan, H., Demir, S., Akyol, C.V., 1992. Prevalence of Paramphistomum species in ruminants of the Marmara region. Doga, Turk Veterinirlik ve Hayvancilik Dergisi 16, 187–197.
Prevalence of Paramphistomum daubneyi infection in cattle in central France V. Szmidt-Adjidéa,1 , M. Abrous a , C.C. Adjidé b , G. Dreyfuss a , A. Lecompte c , J. Cabaret d , D. Rondelaud e,∗ a
Laboratoire de Parasitologie, Faculté de Pharmacie, 2, rue du Docteur Raymond Marcland, 87025 Limoges Cedex, France b Service de Bactériologie-Parasitologie-Virologie, Centre Hospitalier Universitaire, B.P. 465, 97159 Pointe-à-Pitre Cedex, Guadeloupe/F.W.I. c Services Vétérinaires, Abattoir Municipal de Limoges, 125, rue de Nexon, 87000 Limoges Cedex, France d Laboratoire de Parasitologie, Institut National de la Recherche Agronomique, 37380 Nouzilly Cedex, France e Laboratoire d’Histopathologie Parasitaire, Faculté de Médecine, 2, rue du Docteur Raymond Marcland, 87025 Limoges Cedex, France Received 12 January 1999; accepted 14 July 1999
Abstract Investigations at the slaughterhouse of Limoges (Central France) were performed in 1994–1996 to determine the prevalence of Paramphistomum daubneyi infection in cattle. In 1994/1995, higher prevalences of P. daubneyi were recorded in May, October, and January. In 1996, smaller variations were recorded, and prevalence in April and May was higher. The prevalence of P. daubneyi in summer was lower. Breed and age of cattle were not significantly associated to P. daubneyi infection, but females were significantly more infected than males. P. daubneyi infection was related to that of Fasciola hepatica, but not to that of Dicrocoelium lanceolatum. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Cattle-Trematoda; Epidemiology; Paramphistomum daubneyi
1. Introduction Paramphistomes may decrease production in cattle (Spence et al., 1996) and also cause disease (Agosti et al., 1980). Their prevalence has been assessed in most European coun∗
Corresponding author. Present address: Service de Biochimie, Centre Hospitalier Universitaire, B.P. 465, 97159 Pointe-`a-Pitre Cedex, Guadeloupe/F.W.I. 1
0304-4017/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 9 9 ) 0 0 1 6 8 - 5
134
V. Szmidt-Adjid´e et al. / Veterinary Parasitology 87 (2000) 133–138
tries. Several studies had been undertaken in France (Graber et al., 1980, and Casset, 1989, in eastern France; Postal, 1984, in western France). According to Levasseur and Alzieu (1991), the following species occur: Paramphistomum cervi, Paramphistomum daubneyi, Paramphistomum ichikawai, and Paramphistomum microbothrium. P. daubneyi seems to be the more frequent species in cattle. Other trematodes are also recorded in these ruminants such as Fasciola hepatica (Mage and Rondelaud, 1983; Recca and Rivière, 1984) and Dicrocoelium lanceolatum, and they might interfere (positively or negatively) with Paramphistomum infections. We were then interested to assess the prevalence of infection by P. daubneyi in Limousin (central France), a region with relatively high prevalence of F. hepatica infection in cattle.
2. Materials and methods A first investigation at the slaughterhouse of Limoges (department of Haute Vienne, France) was organized from February 1994 to January 1995 on a limited number of cattle in order to estimate monthly variations of prevalence. As this parameter showed large variations in winter and spring, a second study was undertaken from January 1996 to June 1996 to appreciate if these variations were due to small sampling or to a real seasonal variation. In the second investigation, cattle recently treated against F. hepatica (with some whitish calcifications on the surface of the liver) were eliminated. The 1994 average monthly temperature ranged from approximately 5◦ C in December, January, and February to 20◦ C in July and August in Limoges. The yearly rainfall was 1440 mm, and ranged from 200 mm in September to 25 mm in July, in 1994. Paramphistomids found in cattle were P. daubneyi. As the adult worms of the genus Paramphistomum necessitated an histological examination of suckers, we have used the gross morphology and chaetotaxy of the cercaria (Szmidt-Adjidé, 1996), and the local species of the lymnaeid snail (Lymnaea truncatula) used as intermediate host (Szmidt-Adjidé et al., 1994) to identify this paramphistome. The prevalence of infection was recorded using the ratio between the number of infected cattle and that of examined cattle. The intensity of infection in the paunch of cattle was classified into: 0, 1–10, 11–100, 101–200, and more than 200 paramphistomes. In the first investigation, P. daubneyi infection only was studied and the characteristics of hosts were not recorded. In the second investigation, cattle breed, age (younger or older than 2 years), and gender were recorded, and infection with the trematodes D. lanceolatum and F. hepatica were noted. Univariate tests (chi-square, likelihood ratio) were performed with a Simstat software (Péladeau and Lacouture, 1993). The infection odds ratio (OR) and Cornfield interval of confidence at 95% were calculated using software Epi-Info (1991). An OR > 1 indicates that the factors are positively associated with infection. A p value less than 5% was considered statistically significant. The calculations and their rationale are explained by Kleinbaum et al. (1982).
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Table 1 P. daubneyi seasonal prevalence and intensity of infection in cattle from the Limousin region Trial
Sampling month
1994–1995
1996
a b
February March April May June July August September October November December January January February March April May June
Number of cattle examined
52 21 25 20 20 20 25 25 25 25 26 26 170 288 299 203 343 128
Prevalence of infection (%)
0.27 0.10 0.16 0.45 0.15 0.10 0.12 0.08 0.40 0.20 0.19 0.46 0.22 0.21 0.24 0.29 0.29 0.22
Intensity of infectiona (%) Pd 1
Pd 2
Pd 3
Pd 4
0.52 0.50 0.25 0 0 0 0.67 0 0.31 0 0 0.44 0.34 0.28 0.50 0.37 0.26 0.25
0.22 0 0 0.33 0.33 0.33 0 0.50 0.21 0.62 0 0.14 0.48 0.41 0.28 0.47 0.38 0.43
0.15 0 0.50 0.22 0.67 0.67 0.33 0.50 0.31 0 0.19 0.28 0.18 0.20 0.24 0.14 0.32 0.30
0.11b 0.50 0.25 0.45 0 0 0 0 0.17 0.38 0.81 0.14 0 0.01 0.01 0.02 0.04 0.02
Pd 1 (1–10 paramphistomes per ruminant), Pd 2 (11–100), Pd 3 (101–200), Pd 4 (more than 200). Percentage of each class among infected cattle.
3. Results 3.1. Seasonal evolution (Table 1) In 1994/1995, higher prevalence values were recorded in May, October, and January (chi-square or likelihood ratio: p < 0.01). In 1996, smaller variations were recorded and higher prevalences, although non significant (chi-square: p = 0.11), in the first 6 months of the year were found in April and May, which was similar to the preceding investigation (May). When each season was considered, P. daubneyi prevalence was 0.11 in Summer (July, August, and September) instead of 0.30 in Winter, 0.38 in Spring, and 0.36 in Autumn. A statistical difference between these seasons was found (chi-square: p < 0.01), indicating that Summer corresponded to lower infection by P. daubneyi. In 1996, significant differences in the intensity of P. daubneyi infection were found in relation with the month of sampling, May corresponding to the highest infections. 3.2. Host at risk (Table 2) Breed and age were not significantly associated to the prevalence of P. daubneyi infection, whereas gender was significantly associated to prevalence (chi-square: p < 0.01). Females were significantly more frequently infected than males (Odds-ratio OR = 2.17, con-
136
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Table 2 Breed, age, and gender of cattle in relation to the prevalence of trematode infections in the Limousin region, France Breed
Age
Limousine
Less than 2 years
Aquitaine Blonde
More than 2 years Less than 2 years
Frisian a
More than 2 years Less than 2 years More than 2 years
Gender (number of examined cattle)
Female (1016) Male (75) Female (74) Female (68) Male (29) Female (12) Female (114) Female (38)
Prevalence of infectiona P. daubneyi
F. hepatica
D. lanceolatum
0.26 ± 0.03 0.16 ± 0.08 0.23 ± 0.10 0.37 ± 0.12 0.10 ± 0.10 0 0.19 ± 0.37 0.37 ± 0.15
0.07 0.05 0.09 0.09 0 0 0.17 0.05
0.06 0.03 0.05 0.03 0 0 0.01 0.05
Confidence interval at 95%.
fidence interval: 1.20–4.0, p < 0.01). This characteristic was not observed with F. hepatica (OR = 2.29, confidence interval: 0.83–6.33, p = 0.11). No significant differences (chi-squares ranging from 2.2 to 3.3, with significance of p = 0.50–0.30) between the intensities of P. daubneyi infection were recorded in relation to breed, age, gender, or co-infection with other trematodes (data not shown). This means that intensity of infection was not related to any of the factors we studied. 3.3. Trematode associations Prevalence of D. lanceolatum infection was not related to that of P. daubneyi infection. Conversely, prevalences of F. hepatica and of P. daubneyi were correlated (OR = 2.15, confidence interval: 1.44–3.20, p = 0.003).
4. Discussion Prevalence of P. daubneyi infection was on average at 20%, which is much higher than that recorded in one site in France (Casset, 1989; 5.5%), but is similar in another site (Postal, 1984; 14.5%) and to that found in northern Italy (Agosti et al., 1980; 17%) or in Turkey (Tinar et al., 1992; 15%). This might result from actual differences due to different environments, or to an increase in P. daubneyi infection in the last years. Seasonal evolution of infection might be related to climatic variations as shown by Rolfe et al. (1991), depending mostly on rainfall. Rainfall is high in September–October and probably favor cercarial emission in L. truncatula that survived during Summer, which could result into infection of cattle in November–December. Rainfall is also important in January and February, which results into cercaria emission in March and into cattle infection in May. The gender of cattle was the main characteristic that was related to P. daubneyi infection. Females were more infected than males, as already pointed out by Kang and Kim (1988) (68% in females versus 49% in males) or by Asanji (1989). The first explanation concerned
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a longer maintenance of young males in cowshed for a better growth and a faster sale, whereas females rapidly were in pastures, thus leading to higher prevalences. The second point was due to different recruitment of males and females in slaughter houses: females having production or health problems were culled, whereas it was the normal course of production to eliminate males. The positive association between F. hepatica and P. daubneyi is interesting, as Agosti et al. (1980) have already mentioned a co-infection of cattle by these parasites. An argument to explain this parasite association is that both trematodes utilize L. truncatula as an intermediate host. As this snail was living in swampy zones of meadows grazed by cattle, metacercariae of both trematodes were found in the same places and might be ingested together by ruminants. The differences between the prevalence of each trematode infection in cattle might result from the density of metacercariae on grazed grass, or from the specific development of metacercariae in this definitive host.
Acknowledgements The financial help of the Limousin region in the form of a Ph.D. grant to V. Szmidt-Adjidé is gratefully acknowledged.
References Agosti, M., Cavaletti, E., Pozza, O., 1980. Clinica e epizootologia della paramphistomiasi bovina nella Provincia di Milano. Clin. Vet. 103, 284–296. Asanji, M.F., 1989. Paramphistomiasis of cattle in Sierra Leone and seasonal fluctuations in its prevalence. Bull. Anim. Health Prod. Africa 37, 327–331. Casset, I., 1989. Enquête sur la paramphistomose bovine: recherche des parasites en abattoir. Rev. Méd. Vét. 140, 925–927. Epi-Info, 1991. Version 5.01. CDC, Epidemiology Program Office, Atlanta, Georgia, USA. Graber, M., Chauve, C., Fonteneau, M., 1980. Existence en France de Paramphistomum daubneyi Dinnik, 1962. Bull. Acad. Vét. Fr. 53, 265–271. Kang, Y.B., Kim, S.H., 1988. Rumen fluke infections in slaughtered cattle in Korea. Research reports of the rural development administration. Vet. Korean Republic 30, 12–16. Kleinbaum, D.G., Kupper, L.I., Morgenstern, H., 1982. Epidemiologic Research. Van Nostrand Reinhold, New York, 529 p. Levasseur, G., Alzieu, J.P., 1991. La paramphistomose. Bull. Group Tech. Vét. No 404, 153–155. Mage, C., Rondelaud, D., 1983. Réflexions sur la prévention de la fasciolose en France. Dossiers de l’Elevage 5, 25–28. Péladeau, N., Lacouture, Y., 1993. Simstat: boostrap computer simulation and statistical program for IBM personal computer. Behavior Res. Meth. Inst. Comp. 25, 410–413. Postal, J.M., 1984. Les paramphistomoses gastro-duodénales des Ruminants, Vet. Med. Doct. Thesis, Alfort, France, No 164, 125 p. Recca, A., Rivière, F., 1984. Enquête sur la prévalence et la répartition géographique de la fasciolose bovine en France. Bull. Soc. Vét. Prat. 68, 213–242. Rolfe, P.F., Boray, J.C., Nichols, P., Collins, G.H., 1991. Epidemiology of paramphistomosis in cattle. Int. J. Parasitol. 21, 813–819. Spence, S.A., Fraser, G.C., Chang, S., 1996. Response in milk production to the control of gastro-intestinal nematode and paramphistome parasites in dairy cattle. Aust. Vet. J. 74, 456–459.
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