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Parasitic bronchitis in goats and the possible use of Dictyocaulus filaria vaccine for its control
Veterinary Parasitology, 51 (1994) 255-262 0304-4017/94/$07.00 © 1994 - Elsevier Science B.V. All rights reserved
255
Parasitic bronchitis in goats and the possible use of Dictyocaulusfilaria vaccine for its control R.L. Sharma Indian Veterinary Research Institute Campus, Mukteswar-263 138, Nainital, India (Accepted 20 April 1993)
Abstract
Parasitic bronchitis is widely prevalent in migratory flocks of small ruminants in the northwest Himalayan regions of India. The prevalence data collected from 5554 goats, maintained in 31 villages in different agroclimatic regions of the Himalayas, showed that the prevalence of the disease in goats varied from 18.7 to 47.6% with an overall prevalence of 21.8%. Interestingly, 27.6% of goats maintained at an altitude of 2700-3900 m above mean sea level in Kargil (Jammu and Kashmir), where the climate is cold and dry for the major part of the year, were positive for the lungworm infections. The common lungworms observed were Dictyocaulusfilaria, Protostrongylus rufescens, Varestrongylus pneumonicus and occasionally Muellerius spp. The kids were more susceptible to lungworm infections than adult goats. In experimental studies, it was seen that goats were more susceptible to Dictyocaulusfilaria infection than sheep and two vaccine doses comprising 1000 and 2000 gamma-attenuated D. filaria (ovine strain) infective larvae conferred 97% protection in male Beetal kids against a homologous challenge dose of 4200 normal D. filaria larvae. The importance of simultaneous control of the disease in goats and sheep is discussed. Key words: Dictyocaulusfilaria; Muellerius spp.; Protostrongylus rufescens; Goat; Bronchitis; Vaccines; Control methods-Nematoda
Introduction Goat and sheep rearing is the sole source of livelihood for various pastoral nomadic tribes in the Greater Himalayas of India. These flocks regularly ingest developmental stages of parasites while grazing on contaminated pastures during migration to high grasslands in summer (May-September) and whilst returning to their lowland winter grounds in October every year. Amongst various infections which are responsible for low productivity in adults and high mortality in young animals, parasitic bronchitis is an economically important and widely prevalent disease in such hilly regions of India. The control of this disease in sheep in India now relies on a gamma-attenuated Dictyocaulusfilaria vaccine. Nearly half a million lambs, aged 6-8 weeks, have been successfully immunised in endemic areas (Sharma et at., 1988 ). The use of this vaccine in goats is now being considered. The objectives of this paper were therefore to compile available information on the prevalence of the disSSDI 0 3 0 4 - 4 0 1 7 ( 93 ) 0 0 5 3 0 - C
2 56
R.L. Sharrna / Veterinary Parasitology 51 (1994) 255-262
ease in goats and to study the susceptibility of goats to D. filaria infection and their response to D. filaria vaccine under defined laboratory conditions. Materials and methods Studies on the prevalence of lungworm infections in goats were carried out in nomad goat flocks, as well as in Government-owned flocks maintained in the Himalayan belt of Jammu and Kashmir, Himachal Pradesh and Uttar Pradesh. Data on the prevalence of lungworm larvae were collected by coprological examination of fresh faeces of 5554 goats from 31 villages. Pathologic material obtained from slaughterhouses in the endemic areas was also examined for the presence of adult lung worms.
Animals Male Beetal kids and Muzaffarnagri lambs, 4-6 months of age, were utilised for the experiments. These animals were obtained from the hot plains of India and were subjected to both clinical and coprological examination for lungworm and other parasitic infections prior to their use in the experiment. Only those animals found negative for the infection were used for the study. All the experimental animals were housed, stall-fed and maintained on a balanced feeding schedule under strict hygienic conditions throughout the experiment.
Larvae and parasitological techniques The D. filaria larvae required for experimental purposes were obtained from D. filaria producer lambs maintained at this laboratory for vaccine production work. Standard clinicoparasitological techniques used during the course of these investigations have been described elsewhere (Wilson, 1970; Anderson and Verster, 1971; Tewari et al., 1972; Dhar and Sharma, 1978; Sharma et al., 1988 ). Dictyocaulusfilaria infective larvae were irradiated from a 6°Co source (Gamma ceU-900 unit, Isotopes Division, Bhabha Atomic Research Centre, Trombay, Bombay) installed at this laboratory. The exact dose of radiation emitted by the source at the time of irradiation was determined, exposure time was calculated and the larvae, suspended in water, were given the required dose (500 Gy) of gamma radiation. To achieve a uniform ionising effect on the body of the larvae, these were stored for 24 h after irradiation at 4 °C before being administered orally to the experimental animals.
R.L. Sharma / Veterinary Parasitology 51 (1994,) 255-262
2 57
Experiment I An experimental study on the comparative susceptibility of sheep and goats to D. filaria infection was carded out. Animals were divided into two groups: Group 1 consisted of eight kids and Group 2, eight Iambs. Each animal in both groups received an oral infection dose of 1O0 D. filaria infective larvae per kilogram body weight on Day 0. U p o n death, the animals were subject to necropsy and the percentage of adult worms recovered was recorded.
Experiment 2 The immunological response of goats of D. filaria (ovine strain) vaccine was investigated. Animals were allocated to either a vaccinated group or a control group (four animals in each). The vaccination schedule of the former group consisted of two doses of gamma-attenuated D. filaria (ovine strain) larvae: 1000 on Day 0 and 2000 on Day 30. Both groups were challenged on Day 45 with 4200 normal D.filaria infective larvae (a dose rate of 300 larvae per kilogram body weight). The animals in the control group were necropsied upon death, and the day of necropsy, and percentage worm recovery recorded. Animals in the vaccinated group were slaughtered and necropsied on Day 80.
Statistical analysis Statistical analysis of data was done using Student's t-test. A confidence level of 95% or more was considered to be significant. Results
Prevalence Prevalence data on lungworm infections are given in Table 1. The overall prevalence of infection was 21.8% (range 18.7-47.6) with the highest prevalence at Lolab Valley situated in northwest Kashmir. It was interesting to observe that a significant n u m b e r of goats in Kargil district maintained at an altitude of 2700-3900 m above mean sea level (MSL) were positive for lungworms (27.6%). The area has lower precipitation and ambient temperatures than Kashmir Valley. Young animals (less than 6 months of age) had a higher prevalence (30.9%) than adults (24.0%). The majority of animals harboured infections of more than one species of lungworms. The c o m m o n lungworm species encountered during the course of the study were Dictyocaulusfilaria, Protostrongylus rufescens, Varestrongylus pneumonicus and occasionally Muellerius spp.
258
R.L. Sharma / VeterinaryParasitology 51 (1994) 255-262
Table 1 Prevalence of parasitic bronchitis by coprological examination in Indian goats No. of
Survey area
Prevalence of infection
villages No. of animals
Animals positive
LPG t count
No.
Mean
Range
examined
Garhwal Hills (Uttar Pradesh ) Handwara (Kashmir) Lolab Valey (Kashmir) Kargil
%
10
4400
822
18.7
48
0-250
7
198
78
39.4
170
0-450
5
202
96
47.6
211
0-764
9
754
208
27.6
55
0-330
31
5554
1204
21.8
59
0-764
(tadakh)
Overall
'Larvae per gram of faeces.
Table 2 Susceptibility of goats and sheep to Dictyocaulusfilaria (ovine strain) infection (Experiment 1 ) Group
1 (kids) 2 (lambs) 1
No. of animals
8 8
Pre-patent period ( days )
Day of necropsy
Adult worm recovery
Mean
Range
Mean
Range
Mean
%+ SD
27.7 29.9
27-29 28-35
65 65
21-80 34-98
329 297
25.02 + 1.75 17.80+ 1.04
1Sixty-two percent of animals survived the patent infectin.
Experiment 1: Susceptibility Experimental studies on the comparative susceptibility of goats and sheep to D. filaria infection revealed that kids were more susceptible to the infection than lambs (Table 2 ). The percentage adult worm recovery was significantly higher in kids than in lambs ( P < 0.05 ). The kids maintained higher faecal larvae output throughout the period of study than lambs and attained a peak mean larval production of 1100 g-1 faeces during Week 7 post-infection, whereas the corresponding figure for lambs was only 700 g- 1 faeces (Fig. 1 ). However, the prepatent period of the disease was shorter in kids (28 days) than in lambs (30 days). The characteristic signs of parasitic bronchitis were more marked and severe in kids than in lambs. Both species of animals lost body weight (Table 3 ). There were, however, no significant differences in the rate of body weight loss during the first 4 weeks until onset of patency, but thereafter, up to Week 9 post-infection, the kids lost weight at a faster rate
259
R.L. Sharma / Veterinary Parasitology 51 (1994) 255-262
8
"-
g
/" "~\
= ....
~
KIDS LAMBS
X
~4 _J
f
ul
z
8
WEEKS AFTER INFECTION
Fig. 1. Group mean larval production (larvae per gram of faeces, LPG) of lambs and kids (Experiment 1 ). Table 3 Mean ( + SE) body weight (kg) of kids and lambs (Experiment 1 ) Group
No. of Week post-infection animals 0 1
1 (kids) 8 2(lambs) 8
3
5
7
9
11
15.8+0.60 16.0+0.51 14.9+0.47 14.2+0.49 13.5+0.42 13.5+0.47 14.0+0.60 16.6+0.63 16.8+0.73 16.4+0.80 16.2+0.44 16.0+0.41 15.9+0.66 16.0+0.74
than lambs (P<0.05-0.25). These differences became insignificant after Week 9 post-infection. The kids died at intervals following infection, and all had died by the end of the study period, whereas 62% of the lambs survived the acute and patent phase of the infection.
Experiment 2: Immunoprophylaxis The immunological response of goats to D. filaria vaccine was investigated as a pilot study under controlled laboratory conditions. The percentage recovery of worms and clinical course of the disease are given in Table 4. The vaccinated animals were little affected by the challenge infection dose. Only 0.4% of larvae established as adults in vaccinated animals, compared with 15.3% in the unvaccinated controls ( P < 0.001 ). In contrast to the control group, the vaccinated animals had a negligible number of D. filaria larvae in their faeces from Day 30 post-challenge. Clinically, vaccinated animals did not suffer from any characteristic symptom of the disease and maintained a steady gain in body weight, whereas control animals showed characteristic symptoms of the disease and a steep fall in body weight from the 7th week onwards, losing an average of 2-3 kg by the end of experiment. At necropsy, the vaccinated animals showed no lesion except for a few petechial haemorrhages in the apical
260
R.L. Sharma / VeterinaryParasitology 51 (1994) 255-262
Table 4 Vaccination and challenge schedule, worm recovery and prtoection conferred by vaccine in kids (Experiment 2) Group
No. of Vaccination schedule animals Dose 1 Dose 2 (Day 0) (Day 30)
Vaccinated 4 Control 4
1000 ~ -
2000 ~ -
Challenge infection (Day 45)
Necropsy Worm recovery Mean %
Protection conferred (%)
4200 4200
80 29
18 615
97.2 0.0
0.45+0.19 15.34+2.7
~500 Gy, gamma-attenuated D. filaria (ovine strain) infective larvae. The animals in the vaccinated group were slaughtered and necropsied on Day 80; the animals in the control group died and were necropsied on Days 22, 27, 30 and 35.
lobe, but the lungs of control animals revealed characteristic lesions of parasitic bronchitis (Sharma and Bhat, 1990). Discussion
The pioneering report on the occurrence of parasitic bronchitis in Indian goats appeared in the early 1930s (Bhalerao, 1932). Subsequently, the occurrence of the disease has been reported from different parts of the country (Pal, 1978; Sadana et al., 1979; Banerjee and Gupta, 1980), but systematic epizootiological studies on the disease have not been carried out. The prevalence data revealed a fairly high prevalence (21.7%) of the disease which varied from 6 to 92% in different areas, depending upon the climate, migratory pattern and management practices of the flock. The highest prevalence was reported from Lolab Valley, which has a cold and humid climate. Lolab valley has, for most of the year, a congenial climate for the development of freeliving stages of D. filaria and their propagation, transmission and survival (the mean ambient temperature September-June is less than 25 °C and precipitation is 36-104 ram). Low temperature and high humidity are known to be favourable for the development and survival of free-living larvae of D. filaria (Guberlet, 1919; Daubney, 1920; Kauzal, 1933; Rose, 1955 ). Interestingly, a significant number of goats reared at an altitude of 2700-2900 m above MSL in Kargil were positive for the infection. The climate of this region, being cold and dry for major part of the year, is not congenial for the propagation of the majority of parasites of small ruminants. Young kids (less than 6 months of age) had a higher prevalence (30.9%) than adult goats (24.0%). The intensity and incidence of the infection were higher during autumn and winter months. The experimental data reported here on the recovery of adult worms, faecal larval output, severity and clinical course of the disease and mortality following infection and/or vaccination, confirm earlier observations that goats are
R.L. Sharma / VeterinaryParasitology51 (1994) 255-262
261
more susceptible to lungworm infections than sheep (Wilson, 1970; Kassai et al., 1973). In Experiment 2 of this study, the vaccinated animals acquired a strong resistance against a subsequent heavy challenge infection dose of 4200 D. filaria (ovine strain) infective larvae. The control of parasitic bronchitis in sheep through vaccination has become a regular feature of sheep husbandry practice in endemic areas. The impact of the vaccination programme revealed a dramatic fall (3-11%) in the prevalence of infection, when compared with prevalence before the start of the vaccination programme during the 1970s (Sharma et al., 1988 ). However, control of parasitic bronchitis in sheep alone may not fully help in the long run. It seems that the problem cannot be so easily solved, in view of the reported high prevalence of the disease caused by more than one species of lungworms in goats, their susceptibility to the disease and close association with sheep in the endemic areas. Incidentally, goat and sheep suffer from similar species of lungworms and simultaneous control of the disease in goats is therefore unavoidable. The results obtained from experimental studies on the response of goats to D. filaria (ovine strain) vaccine are important, as the use of this radiation-attenuated D. filaria vaccine for the control of the parasitic bronchitis in endemic areas may prove a boon for the overall control of dictyocauliosis in small ruminants. However, it is necessary for the efficacy of the vaccine to be tested in caprines, under the field conditions, before it can be recommended for field use.
Acknowledgements The author wishes to thank S.K. Kaw and K.K. Bhat for their technical help and N.S. Bora for secretarial assistance.
References Anderson, P.S.S. and Verster, A., 1971. Studies on Dictyocaulus filaria. 2. Migration of the developmental Stages in lambs. Onderstepoort J. Vet. Res., 38:185-190. Banerjee, M. and Gupta, P.P., 1980. Incidence and pathology of verminous pneumonia in sheep and goats in the Ludhiana area (Punjab). J. Res. Punjab Agric. Univ., 17: 100-103. Bhalerao, G.D., 1932. On some nematode parasites of goats and sheep at Mukteswar. Indian J. Vet. Sci. Anim. Husb., 2: 242-254. Daubney, R., 1920. The life histories ofDictyocaulusfilaria (Rud) and Dictyocaulus viviparus (Bloch). J. Comp. Pathol. Therap., 33(4): 225-266. Dhar, D.N. and Sharma, R.L., 1978. Dictyocaulusfilaria in lambs: The effect of varying single infections on subsequent larval production. Vet. Parasitol., 4:221-229. Guberlet, E., 1919. On the life history of the lungworm, D. filaria in sheep. J. Am. Vet. Med. Assoc., 55: 621-627. Kassai, T., Altaif, K.I., Kadhim, J.K., Jabbir, M.N. and Bayyar, H.A., 1973. Experiments on the acquired resistance of sheep and goats induced by infections with irradiated and non-irra-
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diated larvae of Dictyocaulusfilaria. Isotopes and Radiations in Parasitology, Vol. III. IAEA, Vienna, pp. 51-60. Kauzal, G., ( 1933 ). Observations on the bionomics of Dictyocaulus filaria with a note on the clinical manifestations in artificial infections in sheep. Aust. Vet. J., 9: 20-26. Pal, N., 1978. Fatal outbreak of verminous pneumonia in caprines. Indian Vet. Med. J., 2: 4850. Rose, J.H., 1955. Observations on the bionomics of the free living larvae of the lungworm Dictyocaulusfilaria. J. Comp. Pathol. Therap., 65:370-381. Sadana, J.R., Purohit, V.D. and Kalra, D.S., 1979. Incidence and pathology of verminous pneumonia in sheep and goats. Haryana Vet., 18:11 l-116. Sharma, R.L. and Bhat, T.K., 1990. Effects ofbronchodilator and intravascular oxygen releaser on the course of Dictyocaulusfilaria infections in lambs. Vet. Parasitol., 35:147-155. Sharma, R.L., Bhat, T.K. and Dhar, D.N., 1988. Control of sheep lungworm in India. Review. Parasitol. Today, 4(2): 33-36. Tcwari, N.C., Rao, Y.V.B.G. and Dhar, D.N., 1972. Studies on radiation-attenuated hclminth vaccines. Laboratory studies on the production and evaluation of gamma irradiated vaccine against the sheep lungworm Dictyocaulusfilaria. Indian J. Anita. Sci., 42: 32-37. Wilson, G.I., 1970. The strength and duration of immunity of Dictyocaulusfilaria infection in sheep and goats. Rcs. Vet. Sci., 11: 7-17.
255
Parasitic bronchitis in goats and the possible use of Dictyocaulusfilaria vaccine for its control R.L. Sharma Indian Veterinary Research Institute Campus, Mukteswar-263 138, Nainital, India (Accepted 20 April 1993)
Abstract
Parasitic bronchitis is widely prevalent in migratory flocks of small ruminants in the northwest Himalayan regions of India. The prevalence data collected from 5554 goats, maintained in 31 villages in different agroclimatic regions of the Himalayas, showed that the prevalence of the disease in goats varied from 18.7 to 47.6% with an overall prevalence of 21.8%. Interestingly, 27.6% of goats maintained at an altitude of 2700-3900 m above mean sea level in Kargil (Jammu and Kashmir), where the climate is cold and dry for the major part of the year, were positive for the lungworm infections. The common lungworms observed were Dictyocaulusfilaria, Protostrongylus rufescens, Varestrongylus pneumonicus and occasionally Muellerius spp. The kids were more susceptible to lungworm infections than adult goats. In experimental studies, it was seen that goats were more susceptible to Dictyocaulusfilaria infection than sheep and two vaccine doses comprising 1000 and 2000 gamma-attenuated D. filaria (ovine strain) infective larvae conferred 97% protection in male Beetal kids against a homologous challenge dose of 4200 normal D. filaria larvae. The importance of simultaneous control of the disease in goats and sheep is discussed. Key words: Dictyocaulusfilaria; Muellerius spp.; Protostrongylus rufescens; Goat; Bronchitis; Vaccines; Control methods-Nematoda
Introduction Goat and sheep rearing is the sole source of livelihood for various pastoral nomadic tribes in the Greater Himalayas of India. These flocks regularly ingest developmental stages of parasites while grazing on contaminated pastures during migration to high grasslands in summer (May-September) and whilst returning to their lowland winter grounds in October every year. Amongst various infections which are responsible for low productivity in adults and high mortality in young animals, parasitic bronchitis is an economically important and widely prevalent disease in such hilly regions of India. The control of this disease in sheep in India now relies on a gamma-attenuated Dictyocaulusfilaria vaccine. Nearly half a million lambs, aged 6-8 weeks, have been successfully immunised in endemic areas (Sharma et at., 1988 ). The use of this vaccine in goats is now being considered. The objectives of this paper were therefore to compile available information on the prevalence of the disSSDI 0 3 0 4 - 4 0 1 7 ( 93 ) 0 0 5 3 0 - C
2 56
R.L. Sharrna / Veterinary Parasitology 51 (1994) 255-262
ease in goats and to study the susceptibility of goats to D. filaria infection and their response to D. filaria vaccine under defined laboratory conditions. Materials and methods Studies on the prevalence of lungworm infections in goats were carried out in nomad goat flocks, as well as in Government-owned flocks maintained in the Himalayan belt of Jammu and Kashmir, Himachal Pradesh and Uttar Pradesh. Data on the prevalence of lungworm larvae were collected by coprological examination of fresh faeces of 5554 goats from 31 villages. Pathologic material obtained from slaughterhouses in the endemic areas was also examined for the presence of adult lung worms.
Animals Male Beetal kids and Muzaffarnagri lambs, 4-6 months of age, were utilised for the experiments. These animals were obtained from the hot plains of India and were subjected to both clinical and coprological examination for lungworm and other parasitic infections prior to their use in the experiment. Only those animals found negative for the infection were used for the study. All the experimental animals were housed, stall-fed and maintained on a balanced feeding schedule under strict hygienic conditions throughout the experiment.
Larvae and parasitological techniques The D. filaria larvae required for experimental purposes were obtained from D. filaria producer lambs maintained at this laboratory for vaccine production work. Standard clinicoparasitological techniques used during the course of these investigations have been described elsewhere (Wilson, 1970; Anderson and Verster, 1971; Tewari et al., 1972; Dhar and Sharma, 1978; Sharma et al., 1988 ). Dictyocaulusfilaria infective larvae were irradiated from a 6°Co source (Gamma ceU-900 unit, Isotopes Division, Bhabha Atomic Research Centre, Trombay, Bombay) installed at this laboratory. The exact dose of radiation emitted by the source at the time of irradiation was determined, exposure time was calculated and the larvae, suspended in water, were given the required dose (500 Gy) of gamma radiation. To achieve a uniform ionising effect on the body of the larvae, these were stored for 24 h after irradiation at 4 °C before being administered orally to the experimental animals.
R.L. Sharma / Veterinary Parasitology 51 (1994,) 255-262
2 57
Experiment I An experimental study on the comparative susceptibility of sheep and goats to D. filaria infection was carded out. Animals were divided into two groups: Group 1 consisted of eight kids and Group 2, eight Iambs. Each animal in both groups received an oral infection dose of 1O0 D. filaria infective larvae per kilogram body weight on Day 0. U p o n death, the animals were subject to necropsy and the percentage of adult worms recovered was recorded.
Experiment 2 The immunological response of goats of D. filaria (ovine strain) vaccine was investigated. Animals were allocated to either a vaccinated group or a control group (four animals in each). The vaccination schedule of the former group consisted of two doses of gamma-attenuated D. filaria (ovine strain) larvae: 1000 on Day 0 and 2000 on Day 30. Both groups were challenged on Day 45 with 4200 normal D.filaria infective larvae (a dose rate of 300 larvae per kilogram body weight). The animals in the control group were necropsied upon death, and the day of necropsy, and percentage worm recovery recorded. Animals in the vaccinated group were slaughtered and necropsied on Day 80.
Statistical analysis Statistical analysis of data was done using Student's t-test. A confidence level of 95% or more was considered to be significant. Results
Prevalence Prevalence data on lungworm infections are given in Table 1. The overall prevalence of infection was 21.8% (range 18.7-47.6) with the highest prevalence at Lolab Valley situated in northwest Kashmir. It was interesting to observe that a significant n u m b e r of goats in Kargil district maintained at an altitude of 2700-3900 m above mean sea level (MSL) were positive for lungworms (27.6%). The area has lower precipitation and ambient temperatures than Kashmir Valley. Young animals (less than 6 months of age) had a higher prevalence (30.9%) than adults (24.0%). The majority of animals harboured infections of more than one species of lungworms. The c o m m o n lungworm species encountered during the course of the study were Dictyocaulusfilaria, Protostrongylus rufescens, Varestrongylus pneumonicus and occasionally Muellerius spp.
258
R.L. Sharma / VeterinaryParasitology 51 (1994) 255-262
Table 1 Prevalence of parasitic bronchitis by coprological examination in Indian goats No. of
Survey area
Prevalence of infection
villages No. of animals
Animals positive
LPG t count
No.
Mean
Range
examined
Garhwal Hills (Uttar Pradesh ) Handwara (Kashmir) Lolab Valey (Kashmir) Kargil
%
10
4400
822
18.7
48
0-250
7
198
78
39.4
170
0-450
5
202
96
47.6
211
0-764
9
754
208
27.6
55
0-330
31
5554
1204
21.8
59
0-764
(tadakh)
Overall
'Larvae per gram of faeces.
Table 2 Susceptibility of goats and sheep to Dictyocaulusfilaria (ovine strain) infection (Experiment 1 ) Group
1 (kids) 2 (lambs) 1
No. of animals
8 8
Pre-patent period ( days )
Day of necropsy
Adult worm recovery
Mean
Range
Mean
Range
Mean
%+ SD
27.7 29.9
27-29 28-35
65 65
21-80 34-98
329 297
25.02 + 1.75 17.80+ 1.04
1Sixty-two percent of animals survived the patent infectin.
Experiment 1: Susceptibility Experimental studies on the comparative susceptibility of goats and sheep to D. filaria infection revealed that kids were more susceptible to the infection than lambs (Table 2 ). The percentage adult worm recovery was significantly higher in kids than in lambs ( P < 0.05 ). The kids maintained higher faecal larvae output throughout the period of study than lambs and attained a peak mean larval production of 1100 g-1 faeces during Week 7 post-infection, whereas the corresponding figure for lambs was only 700 g- 1 faeces (Fig. 1 ). However, the prepatent period of the disease was shorter in kids (28 days) than in lambs (30 days). The characteristic signs of parasitic bronchitis were more marked and severe in kids than in lambs. Both species of animals lost body weight (Table 3 ). There were, however, no significant differences in the rate of body weight loss during the first 4 weeks until onset of patency, but thereafter, up to Week 9 post-infection, the kids lost weight at a faster rate
259
R.L. Sharma / Veterinary Parasitology 51 (1994) 255-262
8
"-
g
/" "~\
= ....
~
KIDS LAMBS
X
~4 _J
f
ul
z
8
WEEKS AFTER INFECTION
Fig. 1. Group mean larval production (larvae per gram of faeces, LPG) of lambs and kids (Experiment 1 ). Table 3 Mean ( + SE) body weight (kg) of kids and lambs (Experiment 1 ) Group
No. of Week post-infection animals 0 1
1 (kids) 8 2(lambs) 8
3
5
7
9
11
15.8+0.60 16.0+0.51 14.9+0.47 14.2+0.49 13.5+0.42 13.5+0.47 14.0+0.60 16.6+0.63 16.8+0.73 16.4+0.80 16.2+0.44 16.0+0.41 15.9+0.66 16.0+0.74
than lambs (P<0.05-0.25). These differences became insignificant after Week 9 post-infection. The kids died at intervals following infection, and all had died by the end of the study period, whereas 62% of the lambs survived the acute and patent phase of the infection.
Experiment 2: Immunoprophylaxis The immunological response of goats to D. filaria vaccine was investigated as a pilot study under controlled laboratory conditions. The percentage recovery of worms and clinical course of the disease are given in Table 4. The vaccinated animals were little affected by the challenge infection dose. Only 0.4% of larvae established as adults in vaccinated animals, compared with 15.3% in the unvaccinated controls ( P < 0.001 ). In contrast to the control group, the vaccinated animals had a negligible number of D. filaria larvae in their faeces from Day 30 post-challenge. Clinically, vaccinated animals did not suffer from any characteristic symptom of the disease and maintained a steady gain in body weight, whereas control animals showed characteristic symptoms of the disease and a steep fall in body weight from the 7th week onwards, losing an average of 2-3 kg by the end of experiment. At necropsy, the vaccinated animals showed no lesion except for a few petechial haemorrhages in the apical
260
R.L. Sharma / VeterinaryParasitology 51 (1994) 255-262
Table 4 Vaccination and challenge schedule, worm recovery and prtoection conferred by vaccine in kids (Experiment 2) Group
No. of Vaccination schedule animals Dose 1 Dose 2 (Day 0) (Day 30)
Vaccinated 4 Control 4
1000 ~ -
2000 ~ -
Challenge infection (Day 45)
Necropsy Worm recovery Mean %
Protection conferred (%)
4200 4200
80 29
18 615
97.2 0.0
0.45+0.19 15.34+2.7
~500 Gy, gamma-attenuated D. filaria (ovine strain) infective larvae. The animals in the vaccinated group were slaughtered and necropsied on Day 80; the animals in the control group died and were necropsied on Days 22, 27, 30 and 35.
lobe, but the lungs of control animals revealed characteristic lesions of parasitic bronchitis (Sharma and Bhat, 1990). Discussion
The pioneering report on the occurrence of parasitic bronchitis in Indian goats appeared in the early 1930s (Bhalerao, 1932). Subsequently, the occurrence of the disease has been reported from different parts of the country (Pal, 1978; Sadana et al., 1979; Banerjee and Gupta, 1980), but systematic epizootiological studies on the disease have not been carried out. The prevalence data revealed a fairly high prevalence (21.7%) of the disease which varied from 6 to 92% in different areas, depending upon the climate, migratory pattern and management practices of the flock. The highest prevalence was reported from Lolab Valley, which has a cold and humid climate. Lolab valley has, for most of the year, a congenial climate for the development of freeliving stages of D. filaria and their propagation, transmission and survival (the mean ambient temperature September-June is less than 25 °C and precipitation is 36-104 ram). Low temperature and high humidity are known to be favourable for the development and survival of free-living larvae of D. filaria (Guberlet, 1919; Daubney, 1920; Kauzal, 1933; Rose, 1955 ). Interestingly, a significant number of goats reared at an altitude of 2700-2900 m above MSL in Kargil were positive for the infection. The climate of this region, being cold and dry for major part of the year, is not congenial for the propagation of the majority of parasites of small ruminants. Young kids (less than 6 months of age) had a higher prevalence (30.9%) than adult goats (24.0%). The intensity and incidence of the infection were higher during autumn and winter months. The experimental data reported here on the recovery of adult worms, faecal larval output, severity and clinical course of the disease and mortality following infection and/or vaccination, confirm earlier observations that goats are
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more susceptible to lungworm infections than sheep (Wilson, 1970; Kassai et al., 1973). In Experiment 2 of this study, the vaccinated animals acquired a strong resistance against a subsequent heavy challenge infection dose of 4200 D. filaria (ovine strain) infective larvae. The control of parasitic bronchitis in sheep through vaccination has become a regular feature of sheep husbandry practice in endemic areas. The impact of the vaccination programme revealed a dramatic fall (3-11%) in the prevalence of infection, when compared with prevalence before the start of the vaccination programme during the 1970s (Sharma et al., 1988 ). However, control of parasitic bronchitis in sheep alone may not fully help in the long run. It seems that the problem cannot be so easily solved, in view of the reported high prevalence of the disease caused by more than one species of lungworms in goats, their susceptibility to the disease and close association with sheep in the endemic areas. Incidentally, goat and sheep suffer from similar species of lungworms and simultaneous control of the disease in goats is therefore unavoidable. The results obtained from experimental studies on the response of goats to D. filaria (ovine strain) vaccine are important, as the use of this radiation-attenuated D. filaria vaccine for the control of the parasitic bronchitis in endemic areas may prove a boon for the overall control of dictyocauliosis in small ruminants. However, it is necessary for the efficacy of the vaccine to be tested in caprines, under the field conditions, before it can be recommended for field use.
Acknowledgements The author wishes to thank S.K. Kaw and K.K. Bhat for their technical help and N.S. Bora for secretarial assistance.
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