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Treatment of inhibited Dictyocaulus viviparus in cattle with ivermectin
Veterinary Parasitology, 25 (1987) 61-66 Elsevier Science PublishersB.V., Amsterdam-- Printed in The Netherlands
T r e a t m e n t of Inhibited Cattle w i t h I v e r m e c t i n
61
Dictyocaulus viviparus in
D. BARTH
Merck Sharp & Dohme Research Laboratories, 8201 Lauterbach ( F.R.G.)
J.M. PRESTON Merck Sharp & Dohme Research Laboratories, Hoddesdon ( Gt. Britain) (Accepted for publication 23 September 1986)
ABSTRACT Barth, D. and Preston, J.M. 1987. Treatment of inhibited Dictyocaulus viviparus in cattle with ivermectin. Vet. Parasitol., 25: 61-66. Fifteencalves,each infectedwith ~ 3000 third stage larvae,wereused to comparethe tendencies of two strains of Dictyocaulus viviparus to inhibit at the fifth larval stage and to evaluate the efficacyof ivermectin.There were notable differencesbetweenthe strains. While> 99% of worms developingfrom infection with an Alpine strain remained inhibited 42 days after infection,only 0-26% of those recoveredfollowinginfectionwith a U.K. laboratorystrain were arrested. Neither adult nor immature D. viviparus were present in the lungs of animals treated with ivermectin subcutaneouslyat 200 ~g/kg body weight 28 days after infection with the Alpine larvae.
INTRODUCTION Inhibited pre-adult stages of Dictyocaulus viviparus in the lungs of cattle were first described in England (Taylor, 1951; Taylor and Michel, 1953). This was followed by reports from Austria ( Supperer and Pfeiffer, 1971 ), Switzerland (Eisenegger and Eckert, 1975), Canada (Gupta and Gibbs, 1975) and Denmark (Jorgensen, 1980). It is assumed t h a t this phenomenon has developed to promote survival of the parasite during the winter period and t h a t under natural conditions the lowered temperatures of the northern hemisphere in a u t u m n influence the free-living third stage larvae which subsequently become inhibited. Only in spring, when the temperature rises again, do the worms develop to m a t u r i t y and act as an important source of infection o n the pasture at the start of the grazing season. Pfeiffer (1976) and Inderbitzin (1976) induced inhibition of D. viviparus in
0304o4017/87/$03.50
© 1987 Elsevier Science Publishers B.V.
62 cattle by storing the third stage larvae at 4-7 °C for 4 weeks before infection, but we were unable to reproduce these findings in a pilot study with a U.K. strain of the parasite. In the present study, the predisposition of two strains of larvae from different geographical areas to inhibit was compared. While adult and normal immature stages of D. viviparus are susceptible to a number of anthelmintics, it is known that inhibited larvae are more resistant to treatment. Fenbendazole orally at 1.5 or 2.0 mg/kg body weight daily for 5 days provided effective control against inhibited stages (Pfeiffer, 1978), but a single dose of 7.5 or 10.0 mg kg- 1 reduced burdens by only 87 and 70%, respectively (Inderbitzin and Eckert, 1978). The efficacy of ivermectin against inhibited D. viviparus was also investigated in the trial reported here. MATERIALSAND METHODS Nine female and six male Fleckvieh cattle aged 6-8 months and reared under worm-free conditions since birth were used. Throughout the study, the animals were individually tied indoors in a manner which precluded accidental acquisition of nematode infection and were fed grass cubes supplemented with a grain-based concentrate. Water was freely available. On the day of infection, the animals were ranked according to body weight and, within replicates of three animals, were allocated randomly to one of three groups. Three replicates comprised female animals and two were males. The animals of Groups 1 and 2 were each infected orally with ~ 3000 third stage D. viviparus larvae of an Alpine strain with a known propensity to inhibit and those of Group 3 were given the same number of larvae of a U.K. strain which had failed to inhibit in a previous probe study. Following collection, the larvae had been stored at 9 ° C for 65 (U.K. strain) or 58 (Alpine strain) days until ~ 1 h before administration, when they were brought to room temperature. During storage, larvae were maintained in water from the same source. Twenty-eight days after infection, the animals of Group 2 were treated with ivermectin 1.0% w/v solution ('IVOMEC' Injection: MSD Agvet) at 200/~g/kg body weight and the animals of Groups 1 and 3 were given an equivalent volume of vehicle solution. Treatments were administered subcutaneously over the shoulder. Individual faecal samples were collected on the day of infection, the day of treatment and 7 and 14 days later. A 20-g sample was examined for the presence of lungworm larvae using a Baermann technique and the number of larvae per gram of faeces (lpg) recorded. Fourteen days after treatment, the animals were slaughtered and the lungs and trachea carefully removed from each. The lungs were perfused with 20 1 water using the method of Inderbitzin (1976) and the worms recovered and enumerated. The lungs were then opened, using scissors, to the level of the bronchioles and any worms present counted. The lungs were minced (4-mm
63 aperture) and a 10%-aliquot digested in a pepsin/HC1 solution with constant stirring for 3-4 hours at 40°C. The resultant suspension was then washed through a 25-pm sieve and the residual worms counted. Worms measuring> 5 mm long were considered adult and those < 5 mm were classified as inhibited pre-adult L5 stages. The numbers of adult and inhibited L5 D. viviparus were transformed to the natural logarithm of ( c o u n t + 1) for analysis and calculation of geometric means. The burdens of the Alpine, control and medicated groups were compared using a t-test for means having unequal variances. Percentage inhibition was calculated individually for each unmedicated animal. RESULTS No adverse reaction to treatment with the vehicle or ivermectin formulations was observed. Clinical signs of parasitic bronchitis such as coughing, dull hair coat and reduced growth were evident only in the unmedicated animals infected with the U.K. strain of D. viviparus. The mean weight gain of this group during the 42 days after infection was 1.2 kg compared with 14.4 kg in the unmedicated group infected with Alpine larvae. During the corresponding period, the animals treated with ivermectin gained an average of 19.2 kg. No D. viviparus larvae were found in the faeces of any of the ivermectintreated animals on any occasion ( Table I). Larvae were recovered from all the animals of Group 3 on the day of treatment and 7 and 14 days later, but only a few larvae were recovered from some of the animals infected with the Alpine strain, suggesting that inhibition had occurred. This was confirmed by the worm burdens at necropsy, which indicated that>99% of the parasites recovered were at the inhibited L5 stage (Table II). In contrast, a much smaller proportion (0-26%) of the U.K. strain was inhibited. No lungworms were found in any of the ivermectin-treated animals, whereas mean burdens of 1.3 adults and 314 inhibited L5 were recovered from the controls infected with the Alpine strain. The difference between the two groups was significant ( P < 0.01 ) for the inhibited stages. DISCUSSION These results show that besides the influence of temperature and age on the ability of third stage larvae to inhibit ( Inderbitzin, 1976; Pfeiffer, 1976), there is also a genetic predisposition, possessed to a greater or lesser extent by different strains. Smeal and Donald (1981) reported similar findings with Ostertagia ostertagi, on the basis of studies with larval populations transferred between a cool tablelands environment and a warm coastal area in New South Wales. Whether D. viviparus strains with a reduced ability to become arrested occur
64 TABLE I Output ofD.
viviparus larvae in faeces of treated and control cattle
Group (infection/treatment)
Animal No.
Larvae per gram of faeces on day~ --28
0
7
14
(I) Alpine larvae:vehicle @ 0.02 ml/kg body weight
309 307 299 295 297
0 0 0 0 0
0 0 0 0 0
0 0.1 0.05 1 0.1
0 0 0 0.2 0
(2) Alpine larvae: ivermectin@ 200 #g/kg body weight
310 305 303 302 296
0 0 0 0 0
0 0 0 0 0
0 0 0 0 0
0 0 0 0 0
(3) U.K. larvae: vehicle @ 0.02 ml/kg body weight
308 306 304 300 298
0 0 0 0 0
63 35 3 9 33
72 183 27 36 144
72 180 1.8 97 96
aDay 0 = day of treatment.
under natural conditions is not known. The U.K. strain described in the present study is that used in the preparation of an irradiated lungworm vaccine (Dictol:Glaxovet) and at the time of investigation it had been maintained under laboratory conditions for ~ 18 years since its initial isolation in Scotland. The Alpine strain, on the other hand, had been passaged only twice in cattle following its collection from the field. Loss of the ability to arrest has also been observed with a strain of O. ostertagi cycled in the laboratory for several years (Armour, 1983). Prolonged storage of larvae of this latter parasite has a similar effect, ascribed by Armour and Bruce (1974), to a selective mortality of the larval population prior to arrest. The complete control of inhibited D. viviparus reaffirms the sensitivity of this parasite to ivermectin, as noted for normally developed immature and adult stages (Benz and Ernst, 1981; Egerton et al., 1981; Lyons et al., 1981; Benz et al., 1984; Armour et al., 1985). Such efficacy will have particular application in areas where overwintering of dictyocaulosis relies heavily on the survival of the parasite within the host, often in the inhibited form. As ivermectin is also highly effective against a range of ectoparasites and gastrointestinal nematodes, including inhibited O. ostertagi, it must be considered a possible treatment of choice for cattle at housing, following a season at grass.
65 TABLE II Burdens of D. viviparus recovered from cattle 14 days after treatment with ivermectin or vehicle solution Group (infection/treatment)
Animal No.
D. viviparus Adults
(I) Alpine larvae:vehicle @ 0.02 ml/kg body weight
309 307 299 295 297 Geometric mean
(2) Alpine larvae: ivermectin @ 200 gg/kg body weight
310 305 303 302 296 Geometric mean
(3) U.K. larvae: vehicle @ 0.02 ml/kg body weight
308 306 304 300 298
Geometric mean
2 3 0 4 0 1.3
InhibitedLs 650 510 210 1080 40 314
0 0 0 0 0
0 0 0 0 0
0
0a
416 293 83 250 215
223
150 60 20 0 10
17.4
aDifferencefrom Group I controlsis statisticallysignificant(P < 0.01). ACKNOWLEDGEMENTS
T h e authors are grateful to Professor Pfeiffer of T h e Institute for Parasitology, V i e n n a a n d Glaxo A n i m a l Health Ltd., for the provision of larvae. Statistical analysis w a s performed by Dr. S.J. Gross.
REFERENCES Armour, J., 1983. Arrested development in cattlenematodes with specialreferenceto Ostertagia ostertagi.In:F.H.M. Borgsteede,Sv.Aa. Henriksen and H.J. Over (Editors),Facts and ReflectionsIII.-Arrested Development of Nematodes in Sheep and Cattle.Central VeterinaryInstitute,Lelystad,The Netherlands,pp. 77-88. Armour, J. and Bruce, R.G., 1974. The inhibitionof development of Ostertagia ostertagi- a diapause phenomenon in a nematode. Parasitology,69: 161-174.
66 Armour, J., Bairden, K., Batty, A.F., Davison, C.C. and Ross, D.B., 1985. Persistent anthelmintic activity of ivermectin in cattle. Vet. Rec., 115: 151-153. Benz, G.W. and Ernst, J.V., 1981. Anthelmintic efficacy of ivermectin against immature gastrointestinal and pulmonary nematodes of calves. Am. J. Vet. Res., 42: 2097-2098. Benz, G.W., Ernst, J.V. and Egerton, J.R., 1984. Anthelmintic activities of ivermectin against immature and adult Dictyocaulus viviparus. Am. J. Vet. Res., 45: 771-772. Egerton, J.R., Eary, C.H. and Suhayda, D., 1981. The anthelmintic efficacy of ivermectin in experimentally infected cattle. Vet. Parasitol., 8: 59-70. Eisenegger, H. and Eckert, J., 1975. Zur Epizootologie und Prophylaxe der Dictyocaulose und den Trichostrongylidosen des Rindes. Schweiz. Arch. Tierheilkd., 117: 255-286. Gupta, R.P. and Gibbs, H.C., 1975. Infection patterns of Dictyocaulus viviparus in calves. Can. Vet. J., 16: 102-108. Inderbitzin, F., 1976. Experimentelle erzeugte Entwicklungshemmung von Dictyocaulus viviparus des Rindes. Diss. Vet. Med., Ziirich. Inderbitzin, F. and Eckert, J., 1978. Die Wirkung von Fenbendazol ( Panacur ~) gegen gehemmte Stadien von Dictyocaulus viviparus und Ostertagia ostertagi bei K~ilbern. Berl. Muench. Tieraerztl. Wochenschr., 91: 395-399. Jorgensen, R.J., 1980. Bovine dictyocaulosis. Pattern of infection and the prevention of parasitic bronchitis. Acta Vet. Scand., 21: 658-676. Lyons, E.T., Tolliver, S.C., Drudge, J.H. and LaBore, D.E., 1981.1: Ivermectin: Controlled test of anthelmintic activity in dairy calves with emphasis on Dictyocaulus viviparus. Am. J. Vet. Res., 42: 1225-1227. Pfeiffer, H., 1976. Zur verzSgerten Entwicklung des Rinderlungenwurms, Dictyocaulus viviparus. Wien. Tieraerztl. Monattschr., 63: 54-55. Pfeiffer, H., 1978. Zur Wirksamkeit von Fenbendazol nach wiederholter Verabreichung niedriger Dosen gegen entwicklungsgehemmte Rinderlungenwtirmer. Wien. Tieraerztl. Monattschr., 65: 343-346. Smeal, M.G. and Donald, A.D., 1981. Effect on inhibition of development of the transfer of Ostertagia ostertagi between geographical regions of Australia. Parasitology, 82: 389-399. Supperer, R. and Pfeiffer, H., 1971. Zur tiberwinterung des Rinderlungenwurms im Wirtstier. Berl. Muench. Tieraerztl. Wochenschr., 84: 386-391. Taylor, E.L., 1951. Parasitic bronchitis in cattle. Vet. Rec., 63: 859-873. Taylor, E.L. and Michel, J.F., 1953. The parasitological and pathological significance of arrested development in nematodes. J. Helminthol., 27: 199-205.
T r e a t m e n t of Inhibited Cattle w i t h I v e r m e c t i n
61
Dictyocaulus viviparus in
D. BARTH
Merck Sharp & Dohme Research Laboratories, 8201 Lauterbach ( F.R.G.)
J.M. PRESTON Merck Sharp & Dohme Research Laboratories, Hoddesdon ( Gt. Britain) (Accepted for publication 23 September 1986)
ABSTRACT Barth, D. and Preston, J.M. 1987. Treatment of inhibited Dictyocaulus viviparus in cattle with ivermectin. Vet. Parasitol., 25: 61-66. Fifteencalves,each infectedwith ~ 3000 third stage larvae,wereused to comparethe tendencies of two strains of Dictyocaulus viviparus to inhibit at the fifth larval stage and to evaluate the efficacyof ivermectin.There were notable differencesbetweenthe strains. While> 99% of worms developingfrom infection with an Alpine strain remained inhibited 42 days after infection,only 0-26% of those recoveredfollowinginfectionwith a U.K. laboratorystrain were arrested. Neither adult nor immature D. viviparus were present in the lungs of animals treated with ivermectin subcutaneouslyat 200 ~g/kg body weight 28 days after infection with the Alpine larvae.
INTRODUCTION Inhibited pre-adult stages of Dictyocaulus viviparus in the lungs of cattle were first described in England (Taylor, 1951; Taylor and Michel, 1953). This was followed by reports from Austria ( Supperer and Pfeiffer, 1971 ), Switzerland (Eisenegger and Eckert, 1975), Canada (Gupta and Gibbs, 1975) and Denmark (Jorgensen, 1980). It is assumed t h a t this phenomenon has developed to promote survival of the parasite during the winter period and t h a t under natural conditions the lowered temperatures of the northern hemisphere in a u t u m n influence the free-living third stage larvae which subsequently become inhibited. Only in spring, when the temperature rises again, do the worms develop to m a t u r i t y and act as an important source of infection o n the pasture at the start of the grazing season. Pfeiffer (1976) and Inderbitzin (1976) induced inhibition of D. viviparus in
0304o4017/87/$03.50
© 1987 Elsevier Science Publishers B.V.
62 cattle by storing the third stage larvae at 4-7 °C for 4 weeks before infection, but we were unable to reproduce these findings in a pilot study with a U.K. strain of the parasite. In the present study, the predisposition of two strains of larvae from different geographical areas to inhibit was compared. While adult and normal immature stages of D. viviparus are susceptible to a number of anthelmintics, it is known that inhibited larvae are more resistant to treatment. Fenbendazole orally at 1.5 or 2.0 mg/kg body weight daily for 5 days provided effective control against inhibited stages (Pfeiffer, 1978), but a single dose of 7.5 or 10.0 mg kg- 1 reduced burdens by only 87 and 70%, respectively (Inderbitzin and Eckert, 1978). The efficacy of ivermectin against inhibited D. viviparus was also investigated in the trial reported here. MATERIALSAND METHODS Nine female and six male Fleckvieh cattle aged 6-8 months and reared under worm-free conditions since birth were used. Throughout the study, the animals were individually tied indoors in a manner which precluded accidental acquisition of nematode infection and were fed grass cubes supplemented with a grain-based concentrate. Water was freely available. On the day of infection, the animals were ranked according to body weight and, within replicates of three animals, were allocated randomly to one of three groups. Three replicates comprised female animals and two were males. The animals of Groups 1 and 2 were each infected orally with ~ 3000 third stage D. viviparus larvae of an Alpine strain with a known propensity to inhibit and those of Group 3 were given the same number of larvae of a U.K. strain which had failed to inhibit in a previous probe study. Following collection, the larvae had been stored at 9 ° C for 65 (U.K. strain) or 58 (Alpine strain) days until ~ 1 h before administration, when they were brought to room temperature. During storage, larvae were maintained in water from the same source. Twenty-eight days after infection, the animals of Group 2 were treated with ivermectin 1.0% w/v solution ('IVOMEC' Injection: MSD Agvet) at 200/~g/kg body weight and the animals of Groups 1 and 3 were given an equivalent volume of vehicle solution. Treatments were administered subcutaneously over the shoulder. Individual faecal samples were collected on the day of infection, the day of treatment and 7 and 14 days later. A 20-g sample was examined for the presence of lungworm larvae using a Baermann technique and the number of larvae per gram of faeces (lpg) recorded. Fourteen days after treatment, the animals were slaughtered and the lungs and trachea carefully removed from each. The lungs were perfused with 20 1 water using the method of Inderbitzin (1976) and the worms recovered and enumerated. The lungs were then opened, using scissors, to the level of the bronchioles and any worms present counted. The lungs were minced (4-mm
63 aperture) and a 10%-aliquot digested in a pepsin/HC1 solution with constant stirring for 3-4 hours at 40°C. The resultant suspension was then washed through a 25-pm sieve and the residual worms counted. Worms measuring> 5 mm long were considered adult and those < 5 mm were classified as inhibited pre-adult L5 stages. The numbers of adult and inhibited L5 D. viviparus were transformed to the natural logarithm of ( c o u n t + 1) for analysis and calculation of geometric means. The burdens of the Alpine, control and medicated groups were compared using a t-test for means having unequal variances. Percentage inhibition was calculated individually for each unmedicated animal. RESULTS No adverse reaction to treatment with the vehicle or ivermectin formulations was observed. Clinical signs of parasitic bronchitis such as coughing, dull hair coat and reduced growth were evident only in the unmedicated animals infected with the U.K. strain of D. viviparus. The mean weight gain of this group during the 42 days after infection was 1.2 kg compared with 14.4 kg in the unmedicated group infected with Alpine larvae. During the corresponding period, the animals treated with ivermectin gained an average of 19.2 kg. No D. viviparus larvae were found in the faeces of any of the ivermectintreated animals on any occasion ( Table I). Larvae were recovered from all the animals of Group 3 on the day of treatment and 7 and 14 days later, but only a few larvae were recovered from some of the animals infected with the Alpine strain, suggesting that inhibition had occurred. This was confirmed by the worm burdens at necropsy, which indicated that>99% of the parasites recovered were at the inhibited L5 stage (Table II). In contrast, a much smaller proportion (0-26%) of the U.K. strain was inhibited. No lungworms were found in any of the ivermectin-treated animals, whereas mean burdens of 1.3 adults and 314 inhibited L5 were recovered from the controls infected with the Alpine strain. The difference between the two groups was significant ( P < 0.01 ) for the inhibited stages. DISCUSSION These results show that besides the influence of temperature and age on the ability of third stage larvae to inhibit ( Inderbitzin, 1976; Pfeiffer, 1976), there is also a genetic predisposition, possessed to a greater or lesser extent by different strains. Smeal and Donald (1981) reported similar findings with Ostertagia ostertagi, on the basis of studies with larval populations transferred between a cool tablelands environment and a warm coastal area in New South Wales. Whether D. viviparus strains with a reduced ability to become arrested occur
64 TABLE I Output ofD.
viviparus larvae in faeces of treated and control cattle
Group (infection/treatment)
Animal No.
Larvae per gram of faeces on day~ --28
0
7
14
(I) Alpine larvae:vehicle @ 0.02 ml/kg body weight
309 307 299 295 297
0 0 0 0 0
0 0 0 0 0
0 0.1 0.05 1 0.1
0 0 0 0.2 0
(2) Alpine larvae: ivermectin@ 200 #g/kg body weight
310 305 303 302 296
0 0 0 0 0
0 0 0 0 0
0 0 0 0 0
0 0 0 0 0
(3) U.K. larvae: vehicle @ 0.02 ml/kg body weight
308 306 304 300 298
0 0 0 0 0
63 35 3 9 33
72 183 27 36 144
72 180 1.8 97 96
aDay 0 = day of treatment.
under natural conditions is not known. The U.K. strain described in the present study is that used in the preparation of an irradiated lungworm vaccine (Dictol:Glaxovet) and at the time of investigation it had been maintained under laboratory conditions for ~ 18 years since its initial isolation in Scotland. The Alpine strain, on the other hand, had been passaged only twice in cattle following its collection from the field. Loss of the ability to arrest has also been observed with a strain of O. ostertagi cycled in the laboratory for several years (Armour, 1983). Prolonged storage of larvae of this latter parasite has a similar effect, ascribed by Armour and Bruce (1974), to a selective mortality of the larval population prior to arrest. The complete control of inhibited D. viviparus reaffirms the sensitivity of this parasite to ivermectin, as noted for normally developed immature and adult stages (Benz and Ernst, 1981; Egerton et al., 1981; Lyons et al., 1981; Benz et al., 1984; Armour et al., 1985). Such efficacy will have particular application in areas where overwintering of dictyocaulosis relies heavily on the survival of the parasite within the host, often in the inhibited form. As ivermectin is also highly effective against a range of ectoparasites and gastrointestinal nematodes, including inhibited O. ostertagi, it must be considered a possible treatment of choice for cattle at housing, following a season at grass.
65 TABLE II Burdens of D. viviparus recovered from cattle 14 days after treatment with ivermectin or vehicle solution Group (infection/treatment)
Animal No.
D. viviparus Adults
(I) Alpine larvae:vehicle @ 0.02 ml/kg body weight
309 307 299 295 297 Geometric mean
(2) Alpine larvae: ivermectin @ 200 gg/kg body weight
310 305 303 302 296 Geometric mean
(3) U.K. larvae: vehicle @ 0.02 ml/kg body weight
308 306 304 300 298
Geometric mean
2 3 0 4 0 1.3
InhibitedLs 650 510 210 1080 40 314
0 0 0 0 0
0 0 0 0 0
0
0a
416 293 83 250 215
223
150 60 20 0 10
17.4
aDifferencefrom Group I controlsis statisticallysignificant(P < 0.01). ACKNOWLEDGEMENTS
T h e authors are grateful to Professor Pfeiffer of T h e Institute for Parasitology, V i e n n a a n d Glaxo A n i m a l Health Ltd., for the provision of larvae. Statistical analysis w a s performed by Dr. S.J. Gross.
REFERENCES Armour, J., 1983. Arrested development in cattlenematodes with specialreferenceto Ostertagia ostertagi.In:F.H.M. Borgsteede,Sv.Aa. Henriksen and H.J. Over (Editors),Facts and ReflectionsIII.-Arrested Development of Nematodes in Sheep and Cattle.Central VeterinaryInstitute,Lelystad,The Netherlands,pp. 77-88. Armour, J. and Bruce, R.G., 1974. The inhibitionof development of Ostertagia ostertagi- a diapause phenomenon in a nematode. Parasitology,69: 161-174.
66 Armour, J., Bairden, K., Batty, A.F., Davison, C.C. and Ross, D.B., 1985. Persistent anthelmintic activity of ivermectin in cattle. Vet. Rec., 115: 151-153. Benz, G.W. and Ernst, J.V., 1981. Anthelmintic efficacy of ivermectin against immature gastrointestinal and pulmonary nematodes of calves. Am. J. Vet. Res., 42: 2097-2098. Benz, G.W., Ernst, J.V. and Egerton, J.R., 1984. Anthelmintic activities of ivermectin against immature and adult Dictyocaulus viviparus. Am. J. Vet. Res., 45: 771-772. Egerton, J.R., Eary, C.H. and Suhayda, D., 1981. The anthelmintic efficacy of ivermectin in experimentally infected cattle. Vet. Parasitol., 8: 59-70. Eisenegger, H. and Eckert, J., 1975. Zur Epizootologie und Prophylaxe der Dictyocaulose und den Trichostrongylidosen des Rindes. Schweiz. Arch. Tierheilkd., 117: 255-286. Gupta, R.P. and Gibbs, H.C., 1975. Infection patterns of Dictyocaulus viviparus in calves. Can. Vet. J., 16: 102-108. Inderbitzin, F., 1976. Experimentelle erzeugte Entwicklungshemmung von Dictyocaulus viviparus des Rindes. Diss. Vet. Med., Ziirich. Inderbitzin, F. and Eckert, J., 1978. Die Wirkung von Fenbendazol ( Panacur ~) gegen gehemmte Stadien von Dictyocaulus viviparus und Ostertagia ostertagi bei K~ilbern. Berl. Muench. Tieraerztl. Wochenschr., 91: 395-399. Jorgensen, R.J., 1980. Bovine dictyocaulosis. Pattern of infection and the prevention of parasitic bronchitis. Acta Vet. Scand., 21: 658-676. Lyons, E.T., Tolliver, S.C., Drudge, J.H. and LaBore, D.E., 1981.1: Ivermectin: Controlled test of anthelmintic activity in dairy calves with emphasis on Dictyocaulus viviparus. Am. J. Vet. Res., 42: 1225-1227. Pfeiffer, H., 1976. Zur verzSgerten Entwicklung des Rinderlungenwurms, Dictyocaulus viviparus. Wien. Tieraerztl. Monattschr., 63: 54-55. Pfeiffer, H., 1978. Zur Wirksamkeit von Fenbendazol nach wiederholter Verabreichung niedriger Dosen gegen entwicklungsgehemmte Rinderlungenwtirmer. Wien. Tieraerztl. Monattschr., 65: 343-346. Smeal, M.G. and Donald, A.D., 1981. Effect on inhibition of development of the transfer of Ostertagia ostertagi between geographical regions of Australia. Parasitology, 82: 389-399. Supperer, R. and Pfeiffer, H., 1971. Zur tiberwinterung des Rinderlungenwurms im Wirtstier. Berl. Muench. Tieraerztl. Wochenschr., 84: 386-391. Taylor, E.L., 1951. Parasitic bronchitis in cattle. Vet. Rec., 63: 859-873. Taylor, E.L. and Michel, J.F., 1953. The parasitological and pathological significance of arrested development in nematodes. J. Helminthol., 27: 199-205.