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The prevalence of patent lungworm infections in herd of dairy cows in the Netherlands
veterinary parasitology ELSEVIER
Veterinary Parasitology 53 (1994) 263-267
The prevalence of patent lungworm infections in herds of dairy cows in the Netherlands M. Eysker*'", E.W. Claessensa, T.J.G.M. Lam b, M.J. Moons ~, A. Pijpers u aDepartment of Parasitology and Tropical Veterinary Medicine, Utrecht University, Yalelaan 1, P.O. Box 80.165, 3508 TD Utrecht, Netherlands bDepartment of Herd Health and Reproduction, Utrecht University, Yalelaan 7, Utrecht, Netherlands (Accepted 31 August 1993)
Abstract
The results of a survey on the prevalence of patent lungworm infections in herds of dairy cows in the Netherlands are presented. Low patent infections were recorded in FebruaryMarch on six out of 40 farms in at least one out of 40 cows. Between mid-April and midJune low patent infections were detected on 28 out of 39 of these farms in one to four of 40 cows. Two farms on which cows were positive in the first round were negative in the second round. One to three positive cows were found on six out of a total of 15 farms revisited in July-August. These results show that lungworm infections are cycled within herds of dairy cows in the Netherlands at a low level. This indicates that dairy cows are important as carriers for lungworm, particularly in spring. The increased patency of lungworm in cows from winter to spring may be explained by maturation of inhibited larvae.
Keywords: Dictyocaulus viviparus; Cattle-Nematoda; Epidemiology-Nematoda;Seasonality; Lungworm disease; Carriers
1. Introduction The pattern of the build-up oflungworm infections in susceptible calves is highly predictable when two factors are known: ( 1 ) when primary infections occur, and (2) the level of these infections (Eysker et al., 1993a,b). An important reason for this predictability is that dispersal ofDictyocaulus viviparus from the dungpat occurs mainly by the fungus Pilobolus (Jorgensen et al., 1982; Somerset al., 1985 ). This fungus translates the larvae very efficiently and most infective larvae reach *Corresponding author. 0304-4017/94/$07.00 © 1994 Elsevier Science BN. All fights reserved SSD10304-4017 (93)00598-S
264
M. Eysker et aL / Veterinary Parasitology 53 (1994) 263-267
the herbage within a week after deposition of the faecal pat (Eysker, 1991 ). This implies reinfection of calves as early as 1 week after the beginning ofpatency. The occurrence of disease in young calves then depends on the 'race' between the buildup of infections and the build-up of immunity. Outbreaks of lungworm disease on commercial farms are difficult to predict because it is usually not known when susceptible animals have acquired their initial infections. Acquisition of overwintered larvae after turnout is not a reliable phenomenon as in gastrointestinal nematodes (Jorgensen, 1981; Eysker et al., 1992). Moreover, it is also uncertain when infections are acquired from carriers and which group serves as the carriers. Previous studies indicate that carrier animals are predominantly found among the yearlings (Jarrett et al., 1955; Enigk and Diiwel, 1962; Biirger, 1978 ). However, a study on 25 outbreaks oflungworm disease on dairy farms around Utrecht, strongly suggested that cows were involved as carriers in a high proportion of analysed cases (Saatkamp et al., 1994). For these reasons a survey was done to study the role of dairy cows as carriers of lungworm.
2. Materials and methods
Forty dairy farms with at least 40 cows from the ambulatory clinic of the Department of Herd Health and Reproduction of the University of Utrecht were selected for the survey. Faecal samples of 40 cows from these farms were collected rectally between l 1 February and 30 March 1992 and again from 39 of the farms between 21 April and 19 June 1992. A third round of faecal sampling of 40 cows was done on 15 'positive' farms between 17 July and 7 August 1992. In the first and second round the initial faecal examination was done using the Baermann method on pooled faecal samples. Faecal samples of 30 g each from 13-14 cows were placed in screens with a diameter of 25 cm and a mesh width of 0.038 mm. Each screen was placed in a container of 30 cm X 40 cm and water was added until the faeces were submerged. After 24 h the screens were removed and the contents of each container were sieved over a screen with a mesh width of 0.020 mm. The debris remaining on this screen was subjected to the 'sucrose interface' procedures described for pasture larval counts (Eysker and Kooyman, 1993). Since approximately 90o/o of the lungworm larvae were recovered with this method it was used throughout the first and second round of sampling. Faeces were stored at 5°C after preparing the 'pooled Baermann' samples. Positive 'pooled Baermann' samples were re-examined individually with the Baermann method (30 g faeces per cow). Sometimes not enough faeces was available to perform this for all cows. In the third round of sampling all cows were examined individually (30 g faeces per cow).
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
265
Table 1 Numbers of lungworm larvae found in pooled Baermann ( 13 or 14 × 30 g faeces) and in individual cows (30 g faeces) No. of larvae
1
2
3
4
5
6
10
14
24
Total
Mass Baermann Cow
29 21
7 2
3 4
2 2
1 0
0 1
0 1
0 1
0 1
42 33
3. Results
3.1. First round of sampling Lungworm larvae were recovered on six of the 40 farms ( 15% ). In all cases one pooled Baermann was positive (5 × 1 and 11 larvae). Re-examination of individual cows confirmed patency of one cow ( 1 larva, 1 larva and 59 larvae per 30 g faeces, respectively) on three farms.
3.2. Second round of sampling Lungworm larvae were found on 28 of the 39 farms (72%). On 14 farms one pooled Baermann was positive and on 14 farms two pooled Baermanns were positive. Re-examination of individual cows confirmed patency for 24 of the 42 patent mass Baermanns. Two farms which were positive in the first round were negative in the second round; thus, the total number of positive farms was 30 out of 39 (77%). When a pooled Baermann is positive it means that at least one patent cow must have been among the 13 or 14 animals examined. This implies that the numbers of patent cows per farm in the second round were at least the numbers found after re-examination plus the numbers of positive pooled Baermanns where no patent cow was found after re-examination. These numbers are: 11 × 0, 14 × 1, 8 × 2, 3 × 3 and 3 × 4. Thus in total at least 51 cows from the 39 herds had patent infections. The numbers of larvae which were recovered from pooled Baermanns and from individual cows after re-examination were usually very low (Table 1 ).
3.3. Third round of sampling In six of the 15 herds (40%) patent cows were found. The numbers of patent cows per herd were 3 × 1, 2 × 2 and 3. The numbers of larvae in the patent cows were 6 × 1, 2, 3, 14 and 23 larvae per 30 g faeces, respectively.
4. Discussion An objection which could be made to the re-examination of the cows is that it has been demonstrated that the recovery of lungworm larvae with the Baermann
266
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
method decreases rapidly when faeces is stored (Cremers, 1981 ). However, other studies (Fox, 1981; M. Eysker, unpublished results, 1990 ) demonstrated that recovery will not decrease when faeces are stored at temperatures of 4-8°C. Fox ( 1981 ) even observed an increase in yield. The present study clearly demonstrates that in a high prevalence area for cattle lungworm like the Netherlands (Boon et al., 1984) low patent infections in some cows will occur on most farms in spring. The percentage of positive farms found is probably an underestimate of the real percentage. In most positive pooled Baermanns or samples from individual cows only one larva was found, which implies that when 30 g faeces are used patent infections in cows may be missed easily. An indication of this is that no positive cows were found after re-examining 21 of the, in total, 48 positive pooled Baermanns and that two positive farms in the first round were negative in the second round. This implies that probably the real proportion of positive dairy cow herds was higher than 77%. An important epidemiological implication of the present findings is that cows are important as carriers for lungworm. This is in line with the results of a retrospective study which indicated that high proportions of cases of lungworm disease may be associated with the cow as carrier (Saatkamp et al., 1994). Jarrett et al. ( 1955 ) and Enigk and Diiwel ( 1962 ) also observed lungworm infections in a low percentage of cows. Because only a low proportion of cows have patent infections and because they excrete low numbers of larvae in their faeces, pasture contamination usually will not be high. This explains why in all the cases where carrier cows were the most likely cause of a lungworm outbreak, disease occurred after one generation of autoinfection of the calves (Saatkamp et al., 1994). Another implication of the results is that lungworm infections are apparently cycled at a low level in dairy cow herds. This is of importance since it allows these herds to maintain immunity even in a closed situation. Influx of lungworm infections through young stock as carriers may not be necessary. The results also indicate an increase in the numbers of patent cows in spring and a decrease again in summer. Most farms were visited in the second round before the cows had been grazing for more than 3 weeks. Since this excludes development of larvae acquired from pasture the most probable explanation for this increase in spring is maturation of inhibited larvae (Supperer and Pfeiffer, 1971 ). The limited third round of sampling was done because in the Netherlands it is much more common to graze calves on pastures used by cows in summer than in spring. Therefore it is relevant to know if cows are equally important as carriers in summer as in spring. The results indicate that this is not so. Nevertheless, a high proportion of herds still contained patent cows in summer.
References Boon, J.I-I., Kloosterman, A. and van der Lende, T., 1984. The incidence of Dictyoeaulus infections in cattle in the Netherlands II: survey of sera collected in the field. Vet. Q., 6:13-17.
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
267
Biirger, H.J., 1978. Survival ofDictyocaulus viviparus in yearling cattle and its significance for pasture contamination in spring. Facts Reflections III: 137-142. Cremers, H.J.W.M., 1981. The correct handling of faecal samples used for examination of Dictyocaulus viviparas larvae. In: P. Nansen, R.J. Jorgensen and E.J.L. Soulsby (Editors), Epidemiology and Control of Nematodiasis in Cattle. Martinus Nijhoff, The Hague, Boston, London, pp. 11-16. Enigk. K. and Diiwel, D., 1962. Beitrag zur Epizootiology der Dictyocaulose des Rindes. Dtsch. Tierarztl. Wochenschr., 69: 72-78. Eysker, M., 1991. Direct measurement of dispersal of Dictyocaulas viviparus in sporangia of Pilobolus spp. Res. Vet. Sci., 50: 29-32. Eysker, M. and Kooyman, F.N.J., 1993. Notes on necropsy and herbage processing techniques for gastrointestinal nematodes of ruminants. Vet. Parasitol., 46:205-213. Eysker, M., Boersema, J.H., Cornelissen, J.B.W.J., Kooyman, F.N.J. and de Leeuw, W.A., 1992. Dictyocaulas viviparus: effect of rotational grazing on the development of infections. Vet. Parasitol., 41: 127-135. Eysker, M., Boersema, J.H., Cornelissen, J.B.W.J., Kooyman, F.N.J., de Leeuw, W.A. and Saatkamp, H.W., 1993a. The effect of rotational grazing for periods of one or two weeks on the build-up of lungworm and gastrointestinal nematode infections in calves. Vet. Q., 15: 20-24. Eysker, M., Saatkamp, H.W. and Kloosterman, A., 1993b. Infection build-up and development of immunity in calves following primary Dictyocaulus viviparus infections of different levels at the beginning or in the middle of the grazing season. Vet. Parasitol., 49: 243-254. Fox, M.T., 1981. Some effects of storage on the recovery of Dictyocaulus viviparus larvae from faeces. In: P. Nansen, R.J. J~rgensen, E.J.L. Soulsby (Editors), Epidemiology and Control of Nematodiasis in Cattle. Martinus Nijhoff, The Hague, Boston, London, pp. 17-20. Jarrett, W.F.H., McIntyre, W.I.M., Urquhart, G.M. and Bell, E.J., 1955. Some factors in the epidemiology of parasitic bronchitis in cattle. Vet. Rec., 67: 820-824. J~rgensen, R.J., 1981. Studies on the lungworm Dictyocaulus viviparus (BIoch, 1792) and its epidemiology in young cattle with a description of an attempt to prevent parasitic bronchitis. Acta Vet. Scand. Suppl., 76: 1-77. J~rgensen, R.J., Ronne, H., Heisted, C. and Iskander, A.R., 1982. Spread of infective Dictyocaulus viviparus larvae in pasture and to grazing cattle: experimental evidence of the role of Pilobolus fungi. Vet. Parasitol., 10: 331-339. Saatkamp, H.W., Eysker, M. and Verhoeff, J., 1994. Study on the causes of outbreaks of lungworm disease on commercial dairy farms in the Netherlands. Vet. Parasitol., 53: 253-261. Somers, C.J., Downey, N.E. and Grainger, J.N.R., 1985. Dispersal of Dictyocaulus viviparus larvae from bovine faeces in Ireland. Vet. Rec., 116: 657-660. Supperer, R. and Pfeiffer, H., 1971. Zur Uberwinterung des Rindedungenwiirmes im Wirtstier. Bed. Muench. Tieraerztl. Wochenschr., 84:386-391.
Veterinary Parasitology 53 (1994) 263-267
The prevalence of patent lungworm infections in herds of dairy cows in the Netherlands M. Eysker*'", E.W. Claessensa, T.J.G.M. Lam b, M.J. Moons ~, A. Pijpers u aDepartment of Parasitology and Tropical Veterinary Medicine, Utrecht University, Yalelaan 1, P.O. Box 80.165, 3508 TD Utrecht, Netherlands bDepartment of Herd Health and Reproduction, Utrecht University, Yalelaan 7, Utrecht, Netherlands (Accepted 31 August 1993)
Abstract
The results of a survey on the prevalence of patent lungworm infections in herds of dairy cows in the Netherlands are presented. Low patent infections were recorded in FebruaryMarch on six out of 40 farms in at least one out of 40 cows. Between mid-April and midJune low patent infections were detected on 28 out of 39 of these farms in one to four of 40 cows. Two farms on which cows were positive in the first round were negative in the second round. One to three positive cows were found on six out of a total of 15 farms revisited in July-August. These results show that lungworm infections are cycled within herds of dairy cows in the Netherlands at a low level. This indicates that dairy cows are important as carriers for lungworm, particularly in spring. The increased patency of lungworm in cows from winter to spring may be explained by maturation of inhibited larvae.
Keywords: Dictyocaulus viviparus; Cattle-Nematoda; Epidemiology-Nematoda;Seasonality; Lungworm disease; Carriers
1. Introduction The pattern of the build-up oflungworm infections in susceptible calves is highly predictable when two factors are known: ( 1 ) when primary infections occur, and (2) the level of these infections (Eysker et al., 1993a,b). An important reason for this predictability is that dispersal ofDictyocaulus viviparus from the dungpat occurs mainly by the fungus Pilobolus (Jorgensen et al., 1982; Somerset al., 1985 ). This fungus translates the larvae very efficiently and most infective larvae reach *Corresponding author. 0304-4017/94/$07.00 © 1994 Elsevier Science BN. All fights reserved SSD10304-4017 (93)00598-S
264
M. Eysker et aL / Veterinary Parasitology 53 (1994) 263-267
the herbage within a week after deposition of the faecal pat (Eysker, 1991 ). This implies reinfection of calves as early as 1 week after the beginning ofpatency. The occurrence of disease in young calves then depends on the 'race' between the buildup of infections and the build-up of immunity. Outbreaks of lungworm disease on commercial farms are difficult to predict because it is usually not known when susceptible animals have acquired their initial infections. Acquisition of overwintered larvae after turnout is not a reliable phenomenon as in gastrointestinal nematodes (Jorgensen, 1981; Eysker et al., 1992). Moreover, it is also uncertain when infections are acquired from carriers and which group serves as the carriers. Previous studies indicate that carrier animals are predominantly found among the yearlings (Jarrett et al., 1955; Enigk and Diiwel, 1962; Biirger, 1978 ). However, a study on 25 outbreaks oflungworm disease on dairy farms around Utrecht, strongly suggested that cows were involved as carriers in a high proportion of analysed cases (Saatkamp et al., 1994). For these reasons a survey was done to study the role of dairy cows as carriers of lungworm.
2. Materials and methods
Forty dairy farms with at least 40 cows from the ambulatory clinic of the Department of Herd Health and Reproduction of the University of Utrecht were selected for the survey. Faecal samples of 40 cows from these farms were collected rectally between l 1 February and 30 March 1992 and again from 39 of the farms between 21 April and 19 June 1992. A third round of faecal sampling of 40 cows was done on 15 'positive' farms between 17 July and 7 August 1992. In the first and second round the initial faecal examination was done using the Baermann method on pooled faecal samples. Faecal samples of 30 g each from 13-14 cows were placed in screens with a diameter of 25 cm and a mesh width of 0.038 mm. Each screen was placed in a container of 30 cm X 40 cm and water was added until the faeces were submerged. After 24 h the screens were removed and the contents of each container were sieved over a screen with a mesh width of 0.020 mm. The debris remaining on this screen was subjected to the 'sucrose interface' procedures described for pasture larval counts (Eysker and Kooyman, 1993). Since approximately 90o/o of the lungworm larvae were recovered with this method it was used throughout the first and second round of sampling. Faeces were stored at 5°C after preparing the 'pooled Baermann' samples. Positive 'pooled Baermann' samples were re-examined individually with the Baermann method (30 g faeces per cow). Sometimes not enough faeces was available to perform this for all cows. In the third round of sampling all cows were examined individually (30 g faeces per cow).
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
265
Table 1 Numbers of lungworm larvae found in pooled Baermann ( 13 or 14 × 30 g faeces) and in individual cows (30 g faeces) No. of larvae
1
2
3
4
5
6
10
14
24
Total
Mass Baermann Cow
29 21
7 2
3 4
2 2
1 0
0 1
0 1
0 1
0 1
42 33
3. Results
3.1. First round of sampling Lungworm larvae were recovered on six of the 40 farms ( 15% ). In all cases one pooled Baermann was positive (5 × 1 and 11 larvae). Re-examination of individual cows confirmed patency of one cow ( 1 larva, 1 larva and 59 larvae per 30 g faeces, respectively) on three farms.
3.2. Second round of sampling Lungworm larvae were found on 28 of the 39 farms (72%). On 14 farms one pooled Baermann was positive and on 14 farms two pooled Baermanns were positive. Re-examination of individual cows confirmed patency for 24 of the 42 patent mass Baermanns. Two farms which were positive in the first round were negative in the second round; thus, the total number of positive farms was 30 out of 39 (77%). When a pooled Baermann is positive it means that at least one patent cow must have been among the 13 or 14 animals examined. This implies that the numbers of patent cows per farm in the second round were at least the numbers found after re-examination plus the numbers of positive pooled Baermanns where no patent cow was found after re-examination. These numbers are: 11 × 0, 14 × 1, 8 × 2, 3 × 3 and 3 × 4. Thus in total at least 51 cows from the 39 herds had patent infections. The numbers of larvae which were recovered from pooled Baermanns and from individual cows after re-examination were usually very low (Table 1 ).
3.3. Third round of sampling In six of the 15 herds (40%) patent cows were found. The numbers of patent cows per herd were 3 × 1, 2 × 2 and 3. The numbers of larvae in the patent cows were 6 × 1, 2, 3, 14 and 23 larvae per 30 g faeces, respectively.
4. Discussion An objection which could be made to the re-examination of the cows is that it has been demonstrated that the recovery of lungworm larvae with the Baermann
266
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
method decreases rapidly when faeces is stored (Cremers, 1981 ). However, other studies (Fox, 1981; M. Eysker, unpublished results, 1990 ) demonstrated that recovery will not decrease when faeces are stored at temperatures of 4-8°C. Fox ( 1981 ) even observed an increase in yield. The present study clearly demonstrates that in a high prevalence area for cattle lungworm like the Netherlands (Boon et al., 1984) low patent infections in some cows will occur on most farms in spring. The percentage of positive farms found is probably an underestimate of the real percentage. In most positive pooled Baermanns or samples from individual cows only one larva was found, which implies that when 30 g faeces are used patent infections in cows may be missed easily. An indication of this is that no positive cows were found after re-examining 21 of the, in total, 48 positive pooled Baermanns and that two positive farms in the first round were negative in the second round. This implies that probably the real proportion of positive dairy cow herds was higher than 77%. An important epidemiological implication of the present findings is that cows are important as carriers for lungworm. This is in line with the results of a retrospective study which indicated that high proportions of cases of lungworm disease may be associated with the cow as carrier (Saatkamp et al., 1994). Jarrett et al. ( 1955 ) and Enigk and Diiwel ( 1962 ) also observed lungworm infections in a low percentage of cows. Because only a low proportion of cows have patent infections and because they excrete low numbers of larvae in their faeces, pasture contamination usually will not be high. This explains why in all the cases where carrier cows were the most likely cause of a lungworm outbreak, disease occurred after one generation of autoinfection of the calves (Saatkamp et al., 1994). Another implication of the results is that lungworm infections are apparently cycled at a low level in dairy cow herds. This is of importance since it allows these herds to maintain immunity even in a closed situation. Influx of lungworm infections through young stock as carriers may not be necessary. The results also indicate an increase in the numbers of patent cows in spring and a decrease again in summer. Most farms were visited in the second round before the cows had been grazing for more than 3 weeks. Since this excludes development of larvae acquired from pasture the most probable explanation for this increase in spring is maturation of inhibited larvae (Supperer and Pfeiffer, 1971 ). The limited third round of sampling was done because in the Netherlands it is much more common to graze calves on pastures used by cows in summer than in spring. Therefore it is relevant to know if cows are equally important as carriers in summer as in spring. The results indicate that this is not so. Nevertheless, a high proportion of herds still contained patent cows in summer.
References Boon, J.I-I., Kloosterman, A. and van der Lende, T., 1984. The incidence of Dictyoeaulus infections in cattle in the Netherlands II: survey of sera collected in the field. Vet. Q., 6:13-17.
M. Eysker et al. / Veterinary Parasitology 53 (1994) 263-267
267
Biirger, H.J., 1978. Survival ofDictyocaulus viviparus in yearling cattle and its significance for pasture contamination in spring. Facts Reflections III: 137-142. Cremers, H.J.W.M., 1981. The correct handling of faecal samples used for examination of Dictyocaulus viviparas larvae. In: P. Nansen, R.J. Jorgensen and E.J.L. Soulsby (Editors), Epidemiology and Control of Nematodiasis in Cattle. Martinus Nijhoff, The Hague, Boston, London, pp. 11-16. Enigk. K. and Diiwel, D., 1962. Beitrag zur Epizootiology der Dictyocaulose des Rindes. Dtsch. Tierarztl. Wochenschr., 69: 72-78. Eysker, M., 1991. Direct measurement of dispersal of Dictyocaulas viviparus in sporangia of Pilobolus spp. Res. Vet. Sci., 50: 29-32. Eysker, M. and Kooyman, F.N.J., 1993. Notes on necropsy and herbage processing techniques for gastrointestinal nematodes of ruminants. Vet. Parasitol., 46:205-213. Eysker, M., Boersema, J.H., Cornelissen, J.B.W.J., Kooyman, F.N.J. and de Leeuw, W.A., 1992. Dictyocaulas viviparus: effect of rotational grazing on the development of infections. Vet. Parasitol., 41: 127-135. Eysker, M., Boersema, J.H., Cornelissen, J.B.W.J., Kooyman, F.N.J., de Leeuw, W.A. and Saatkamp, H.W., 1993a. The effect of rotational grazing for periods of one or two weeks on the build-up of lungworm and gastrointestinal nematode infections in calves. Vet. Q., 15: 20-24. Eysker, M., Saatkamp, H.W. and Kloosterman, A., 1993b. Infection build-up and development of immunity in calves following primary Dictyocaulus viviparus infections of different levels at the beginning or in the middle of the grazing season. Vet. Parasitol., 49: 243-254. Fox, M.T., 1981. Some effects of storage on the recovery of Dictyocaulus viviparus larvae from faeces. In: P. Nansen, R.J. J~rgensen, E.J.L. Soulsby (Editors), Epidemiology and Control of Nematodiasis in Cattle. Martinus Nijhoff, The Hague, Boston, London, pp. 17-20. Jarrett, W.F.H., McIntyre, W.I.M., Urquhart, G.M. and Bell, E.J., 1955. Some factors in the epidemiology of parasitic bronchitis in cattle. Vet. Rec., 67: 820-824. J~rgensen, R.J., 1981. Studies on the lungworm Dictyocaulus viviparus (BIoch, 1792) and its epidemiology in young cattle with a description of an attempt to prevent parasitic bronchitis. Acta Vet. Scand. Suppl., 76: 1-77. J~rgensen, R.J., Ronne, H., Heisted, C. and Iskander, A.R., 1982. Spread of infective Dictyocaulus viviparus larvae in pasture and to grazing cattle: experimental evidence of the role of Pilobolus fungi. Vet. Parasitol., 10: 331-339. Saatkamp, H.W., Eysker, M. and Verhoeff, J., 1994. Study on the causes of outbreaks of lungworm disease on commercial dairy farms in the Netherlands. Vet. Parasitol., 53: 253-261. Somers, C.J., Downey, N.E. and Grainger, J.N.R., 1985. Dispersal of Dictyocaulus viviparus larvae from bovine faeces in Ireland. Vet. Rec., 116: 657-660. Supperer, R. and Pfeiffer, H., 1971. Zur Uberwinterung des Rindedungenwiirmes im Wirtstier. Bed. Muench. Tieraerztl. Wochenschr., 84:386-391.