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Prevalence of coccidia in sheep in Zimbabwe
SrnallRuminant Research, 8 (1992) 257-264 © 1992 Elsevier Science Publishers B.V. All rights reserved. 0921-4488/92/$05.00
257
Prevalence of coccidia in sheep in Zimbabwe R.C. Chhabra and V.S. Pandey Department of Paraclinical Veterinary Studies, University of Zimbabwe, Mount Pleasant, Harare. Zimbabwe (Accepted 24 September 1991 )
ABSTRACT Chhabra, R.C. and Pandey, V.S., 1992. Prevalence of coccidia in sheep in Zimbabwe. Small Rumin. Res., 8: 257-264. A total of 497 domestic sheep faecal samples, from three farms in Zimbabwe, were collected per rectum between February 1989 and March 1990 to survey intestinal coccidia. Number of oocysts per gram (OPG) of faeces was determined by the standard McMaster technique and identification of oocysts was done on sporulation. On average, 83.3% (range 72.8-92.8%) of samples were positive for coccidia oocysts. Among the positives, OPG was < 1000 in 71% of samples, 1500-5000 in 22%, 500010 000 in 3.6%, and above 10 000 in 3.4% of samples. The highest recorded OPG was 118 800. Animals showing counts over 10 000 OPG revealed a significant drop when examined after a month. Eleven species ofcoccidia were identified from 122 individual samples. Eimeria ovinoidalis ( =E. ninakohlyakimovae) was the most prevalent species, found in all animals, followed by E. parva (98.3%), E. ovina (95.0%), E. ahsata (91.0%), E. crandallis (69.7%), E. faurei (61.4%), E. granulosa (53.2%), E. caprovina (26.2%), E. pallida (24.6%), E. intrictata (23.8%) and E. christenseni (12.3%). E. ovinoidalis was the most predominant species, showing the highest counts in 59 sheep (48.4%). Of the 122 samples, 84% had five to eight species ofcoccidia. All species are reported for the first time from Zimbabwe.
INTRODUCTION
Eimeria species of coccidia are ubiquitous parasites occuring in many species of domestic animals, including sheep. A high prevalence of mixed infections by a number of Eimeria species has been reported in sheep from many countries (McKenna, 1972; Pout, 1973; Mason, 1977; Vercruysse, 1982; Gregory and Catchpole, 1987; Pandit et al., 1987; Manzhos et al., 1988 ). Eimeria species of sheep and goats shown earlier as identical are now considered as separate species on the basis of host-specificity experiments in these animals (McDougald, 1979; Sayin et al., 1980) and reviewed by Norton ( 1986 ). Coccidiosis caused by Eimeria species in sheep is an important intestinal condiCorrespondence to: V.S. Pandey, Institute of Tropical Medicine, Department of Tropical Animal Production and Health, Nationalestraat, 155, B-2000 Antwerp 1, Belgium.
258
R.C. CHHABRA AND V.S. PANDEY
tion, outbreaks in lambs causing high morbidity and mortality (Salisbury et al., 1953; Rusev, 1987; Manzhos et al., 1988). As there was no information available on coccidia of sheep in Zimbabwe and the relevance of work done in other countries to Zimbabwean conditions is doubtful, the present study was carried out to study the prevalence and intensity of coccidia in sheep in Zimbabwe. MATERIALS AND METHODS
Study sites The study was carried out in sheep at three farms, two within 20 km of Harare, namely 'U.Z.' and 'Siddiqui' and one at Makoholi, located about 250 km south of Harare. The climate of Harare is generally moderate with a warm, wet period from November to April and a mean annual rainfall of 800 m m , a cool dry period from May to August, and a hot, dry period from September to October/November. M a x i m u m mean monthly temperature of 29 ° C is recorded in October and m i n i m u m mean monthly temperature of 6.5 °C in July. The climate of Makoholi is drier than that of Harare, with a mean annual rainfall of 650 mm.
Animals The sheep were of the indigenous breed with some at Makoholi being crosses of indigenous × Merino. Each flock was run as a unit and grazed natural pastures with supplements during the dry season. Animals did not receive anticoccidial drugs during the study period. The age of the animals was from 4 months to adult. To determine the earliest natural infection with coccidia, six lambs separated from their coccidia-infected mothers 24-48 h after birth were maintained in cages under coccidia-free conditions and their faeces examined at 1- or 2-day intervals.
Faecal examination Faecal samples were collected per rectum in plastic bags from February 1989 to March 1990, and kept in a refrigerator at 4 °C until processed. A total of 497 faecal samples were examined. N u m b e r of oocysts per gram ( O P G ) of faeces was determined by the standard McMaster technique (Soulsby, 1982 ) to an accuracy of 1 oocyst counted, representing 50 oocysts per g of faeces.
Identification of species of coccidia Identification of Eimeria species was carried out on 122 individual faecal samples after sporulation in 2.5% potassium dichromate solution (McKenna, 1972 ). Oocysts were concentrated by centrifugal flotation using saturated sod i u m chloride solution (Soulsby, 1982 ). They were identified under a 40X, and at times a 100X objective. Usually 100 oocysts were identified from each
PREVALENCE OF COCCIDIA IN SHEEP IN ZIMBABWE
259
faecal sample. Measurements of oocysts were taken with a calibrated ocular micrometer under a 40X objective. For identification, various figures and descriptions given by earlier workers (Shah, 1963; Joyner et al., 1966; Pellerdy, 1974; Levine, 1985; Norton, 1986) were used, although at times it was subjective. RESULTS
Between 72.8 and 92.9% of samples examined were positive for Eimeria oocysts (Table 1 ). Over two-thirds of infected sheep had OPG less than 1000, and only 0.7% had over 50 000. Mean oocyst counts varied from 1256 to 1768, and the maximum recorded OPG was 118 800 (Table 2 ). There was no difference between the prevalence of coccidia of indigenous and crossbred sheep, but intensity of infection was higher in crossbred sheep. There appeared to be no important seasonal variation in oocyst counts. There was, however, marked fluctuation in oocyst counts of individuals examined at monthly intervals. A significant drop in TABLE 1 Prevalence of coccidia oocysts in faecal samples from sheep at three farms in Zimbabwe Farm
Number examined
Number positive (% positive )
Makoholi Siddiqui U.Z.
213 116 168
155 (72.8) 103 (88.8) 156 (92.9)
Total
497
414 (83.3)
TABLE2
Eimeriaoocystspergram(OPG) of~ecesinsheepatthree~rmsinZimbabwe RangeofOPG
50-950 1000-4950 5000-9950 10 000-49 950 50 000-99 950 Over 100 000 Mean OPG of all samples Max. OPG recorded
Percentage of infected sheep Makoholi
Siddiqui
76.8 20.6 0.7 0.7 0.6 0.6 1256 118 800
70.9 20.4 2.9 5.8 -
-
1768 48 600
Total
U.Z. 65.4 24.4 7.0 2.6 0.6 -
1293 29 000
71.0 22.0 3.6 2.7 0.5 0.2 1480 -
260
R.C. CHHABRAAND V.S.PANDEY
count was registered in animals showing OPG over l 0 000, and at times no oocysts were found in faeces of an individual re-examined after a month. A total of 11 species of Eimeria were identified. Percentages of animals harbouring different species are shown in Table 3. All samples had mixed infections with 3-10 species, and over 50% had 6-7 species (Table 4). E. ovinoidalis ( = E. n inakohlyakimovae) was the most predominant species, with highest counts in 48.4% of 122 sheep, followed by E. parva in 20.5%, E. ahsata in 12.3% and E. ovina in 8.2% of sheep (Table 5). Two species, E. crandallis TABLE 3 Prevalence rate (no. positive/no, examined× 100) of Eimeria species in sheep at three farms in Zimbabwe Eimeria species
Prevalence rate (%)
Makoholi
E. ovinoidalis E. parva E. ovina E. ahsata E. crandallis E. faurei E. granulosa E. caprovina E. pallida E. intricata E. christenseni
Siddiqui ( n = 14)
U.Z. (n=49)
Total
( n = 59) 1O0 98 95 98 73 56 56 22 29 19 19
I O0 93 93 93 100 43 43 57 0 28 14
1O0 100 96 82 57 73 53 22 27 29 4
1O0 98 95 91 70 61 53 26 25 24 12
( n = 122)
TABLE 4 Number o f Eimeria species in mixed infections in sheep at three farms in Zimbabwe Number o f Eimeria species
Three Four Five Six Seven
Eight Nine Ten
Percentage of samples infected Makoholi (n=59)
Siddiqui ( n = 14)
U.Z. (n=49)
Total
0 3.4 13.6 25.4 28.8 16.9 10.2 1.7
0 0 7.1 50.0 7.1 21.5 14.0 0
4.1 6.1 16.3 24.5 26.5 14.3 6.2 2.0
1.6 4.0 14.0 28.0 25.4 16.4 9.0 1.6
( n = 122)
PREVALENCE OF COCCIDIA IN SHEEP IN ZIMBABWE
261
TABLE 5 P r e d o m i n a n t E i m e r i a species in sheep at three f a r m s in Z i m b a b w e E i m e r m species
E. ovinoidalis E. parva E. ovina E. ahsata E.faurei E. granulosa E. caprovina E. pallida E. intricata
P r e d o m i n a n c e rate (%) Makoholi (n=59)
Siddiqui ( n = 14)
U.Z, (n=49)
Total ( n = 122)
40.6 32.2 3.4 15.3 6.8 1.7
50.0 7.1 14.3 14.3 7.1 7.1
57.1 10.2 12.2 8.2 2.0 4.1 4.1 2.0
48.4 20.5 8.2 12.3 0.8 4.9 0.8 1.6 2.5
and E. christenseni, did not have highest counts in any of the 122 samples examined. In the six lambs separated from their mothers 24-48 h after birth, Eimeria oocysts were detected for the first time when they were 18-28 days old. DISCUSSION
Prevalence of infection in sheep in the present study (Table 1 ) was similar to the infection rates of up to 95% recorded in other countries (Michael and Probert, 1970; McKenna, 1972; Catchpole et al., 1975; Vercruysse, 1982), but higher than the 69% recorded in Illinois, U.S.A. by Shah ( 1963 ). Although the majority of animals had oocyst counts below 1000 and the mean count of the three farms was 1480, a small proportion of sheep had very high counts (Table 2), and it is mainly these animals which contributed to heavy contamination of the environment. A similar phenomenon, that a few animals in an infected flock produce a large number of eggs, is known to occur in trichostrongylid nematodes of sheep (Windon, 1990 ). As reported by Pout and Ostler ( 1966 ) and Mason ( 1977 ), the present study also revealed marked fluctuation in faecal oocyst count of individuals examined at monthly intervals. Gregory and Catchpole (1987 ) claimed that oocyst counts done three days apart could be quite unrelated in numbers, heavily infected animals showing a drop in OPG when examined a month later. Similar observations were made in goats from the same areas of Zimbabwe (Chhabra and Pandey, 1991 ). According to Davies et al. ( 1963 ) and Mason ( 1977 ), with increasing infective dose of oocysts a point is reached where inhibition of oocysts occurs, resulting in decreased faecal oocyst output. However, the fluctuation in oocyst
262
R.C. CHHABRA AND V.S. P A N D E r
output may be due to local immune response (Barriga, 1981 ), circadian rhythm, and age (Pout, 1973; Mason, 1977). Crossbreds of indigenous × Merino sheep had a higher intensity of infection, as was the case with coccidial infection of crossbred goats from the same locality (Chhabra and Pandey, 1991 ). E. ovinoidalis, E. parva, E. ovina ( = E. arloingi ) and E. ahsata, which were present in 90-100% of sheep with high predominance (Tables 3 and 5 ), are reported to be very pathogenic and may cause overt coccidiosis (Lotze, 1954; Smith et al., 1960; Horton and Stockdale, 1979; Manzhos et al., 1988; Gregory et al., 1989 ). Mixed infection with several species of coccidia (Table 4) is the rule in natural infections, although the number and composition of species may vary (Michael and Probert, 1970; Mason, 1977). The first appearance ofoocysts at the age of 18-28 days in lambs separated from their mothers 24-48 h after birth and thereafter kept in coccidia free conditions, supports the view that lambs can pick up infectionjust after birth, probably from their mother's udder or body, and become patent in the first 3-5 weeks of life (Pout and Ostler, 1966; Mason, 1977). In conclusion, it may be stated that the prevalence of coccidia in sheep in Zimbabwe is high. Out of 11 species reported, the prevalence and predominance of known pathogenic species is high and coccidiosis as a disease entity in sheep in Zimbabwe merits further investigation. ACKNOWLEDGEMENTS
Thanks are due to the technical staff of the Parasitology Laboratory of the Department of Paraclinical Veterinary Studies for their able assistance, to the different farms for the collection of samples, and for the grant provided by the Research Board, University of Zimbabwe, to carry out this work. REFERENCES Barriga, O.O., 1981. The immunology of parasitic infections. A Handbook for Physicians, Veterinarians and Biologists. University Park Press, Baltimore, 354 pp. Catchpole, J., Norton, C.C. and Joyner, L.P., 1975. The occurrence of Eimeria weybridgensis and other species of coccidia in lambs in England and Wales. Br. Vet. J., 131:392-401. Chhabra, R.C. and Pandey, V.S., 1991. Coccidia of goats in Zimbabwe. Vet. Parasitol., 39:199205. Davies, S.M.F., Joyner, L.P. and Kendall, S.B., 1963. Coccidiosis. Oliver and Boyd, London, 264 pp. Gregory, M.W. and Catchpole, J., 1987. Output of coccidial oocysts (particularly Eirneria crandallis) by naturally infected lambs: daily and hourly patterns and clinical significance. Dtsch. Tier~irztl. Wochenschr., 94:521-525. Gregory, M.W., Catchpole, J., Nohan, A. and Herbert, C.N., 1989. Ovine coccidiosis: studies on the pathogenicity of Eimeria ovinoidalis and E. crandallis in conventionally-reared lambs, including possible effects of passive immunity. Dtsch. Tier~irztl. Wochenschr., 96: 287-292.
PREVALENCE OF COCCIDIA IN SHEEP IN ZIMBABWE
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Horton, G.M.J. and Stockdale, P.H.G., 1979. Effects of amprolium and monensin on oocyst discharge, feed utilization, and ruminal metabolism of lambs with coccidiosis. Am. J. Vet. Res., 40: 966-970. Joyner, L.P., Norton, C.C., Davies, S.F.M. and Watkins, C.V., 1966. The species of coccidia occurring in cattle and sheep in the South-West of England. Parasitology, 56:531-541. Levine, N.D., 1985. Veterinary Protozoology. 1st Edn. Iowa State University Press, Ames, IA, 414pp. Lotze, J.C., 1954. The pathogenicity of the coccidian parasite, Eimeria ninakohlyakimovae (Yakinov and Rastegaieff, 1930 ) in domestic sheep. Proc. Am. Vet. Med. Assoc., 1953:141 146.
Manzhos, A.F., Prikhod'ko, Yu.A., Sumtsov, V.S. and Kolomatskii, A.P., 1988. Eimeria infection in sheep: epidemiology, diagnosis and economic losses. Veterinariya, Moscow, 7: 3437. Mason, P., 1977. Naturally acquired coccidia infection in lambs in Otago. N. Z. Vet. J., 25: 3033. McDougald, L.R., 1979. Attempted cross-transmission of coccidia between sheep and goats and description of Eimeria ovinoidalis (sp.n.). J. Protozool., 26:109-113. McKenna, P.B., 1972. The identity and prevalence of coccidia species in sheep and cattle in New Zealand. N. Z. Vet. J., 20: 225-228. Michael, E. and Probert, J., 1970. The prevalence of coccidia in faecal samples from sheep in North Wales. Res. Vet. Sci., 11: 402-405. Norton, C.C., 1986. Coccidia of the domestic goat Capra hircus, with notes on Eimeria ovinoidalis and E. bakuensis (syn. E. ovina) from the sheep Ovis aries. Parasitology, 92: 279-289. Pandit, B.A., Prasad, K.D. and Sahai, B.N., 1987. Prevalence of Eimeria infections in sheep of Chotanagpur, Bihar. J. Vet. Parasitol., 1:71-75. Pellerdy, L.P., 1974. Coccidia and Coccidiosis. 2nd Edn. Paul Parey, Berlin, 959 pp. Pout, D.D., 1973. Coccidiosis of lambs: 1. Observations on the naturally acquired infection. Br. Vet. J., 129: 555-567. Pout, D.D. and Ostler, D.C., 1966. The coccidial population in clinically normal sheep. Vet. Rec., 78: 455-460. Rusev, I., 1987. Treatment and prophylaxis of coccidiosis in lambs and kids. Veterinarna Sbirka, 85: 17-18. Salisbury, R.M., Muir, J. and Stifling, J., 1953. Coccidiosis as a probable cause of unthriftiness and deaths in lambs. N. Z. Vet. J., 1: 72-77. Sayin, F., Dincer, S. and Milli, U., 1980. The life cycle and pathogenicity of Eimeria arloingi (Marotel, 1905) Martin, 1909 in Angora kids and an attempt at its transmission to lambs. Zentralbl. Vet. Med., Reihe B., 27: 382-397. Shah, H.L., 1963. Coccidia (Protozoa: Eimeriidae) of the domestic sheep in the United States, with descriptions of the sporulated oocysts of six species. J. Parasitol., 49: 799-807. Smith, W.N., Davies, L.R. and Bowman, G.W., 1960. The pathogenicity of Eimeria ashata, a coccidium of sheep. J. Protozool., 7: Suppl., 8. Soulsby, E.J.L., 1982. Helminths, Arthropods and Protozoa of Domesticated Animals. 7th Edn., Bailliere Tindall, London, 809 pp. Vercruysse, J., 1982. The coccidia of sheep and goats in Senegal. Vet. Parasitol., 10: 297-306. Windon, R.G., 1990. Selective breeding for the control ofnematodiasis in sheep. Rev. Sci. Tech. Off. Int. Epiz., 9: 555-576. RESUME Chhabra, R.G. et Pandey, V.S., 1992. Pr6valence de la coccidie chez les moutons au Zimbabwe. SmalI Rurnin. Res., 8: 257-264.
264
R.C. CHHABRAAND V.S.PANDEY
De f6vrier 1989 h mars 1990, 497 6chantillons de mati~res f6cales, r6colt6s directement au niveau du rectum de moutons provenant de trois fermes au Zimbabwe, ont 6t~ examin6s pour la recherche des coccidies intestinales. Le nombre de oocysts par g de f~ces (OPG) 6tait 6valu6 par la technique classique de McMaster, et les oocysts ont 6t6 identifi6s apr~s leur sporulation. En moyenne 83.3% (extremes 72.8-92.8%) des 6chantillons 6taient positifs pour la coccidioses. Parmi les 6chantillons positifs, 71% avaient un OPG de moins de 1000, 3.6% de 1500 h 5000 et 3.4% de plus de 10 000. L'OPG le plus 61ev6 6tait de 118 800. Les animaux avec un OPG de plus de 10 000 examin6s un mois plus tard, ont montr~ une diminution significative du nombre d'oocysts dans leur f~ces. Un examen de 122 6chantillons individuels a permis l'identification de 11 esp~ces diff6rentes de coccidies. Eimeria ovinoidalis ( =E. ninakohlyakirnovae) 6tait l'esp~ce la plus fr6quente et fur rencontr6e dans 100% des 6chantillons. Elle 6tait suivie de E. parva (98.3%), E. ovina (95.0%), E. ahsata (91.0%), E. crandallis (69.7%), E. faurei (61.4%), E. granulosa (53.2%), E. caprovina (26.2%), E. pallida (24.6%), E. intricata (23.8%) et E. christenseni (12.3%). E. ovinoidalis 6tait l'esp~ce la plus dominante, avec I'OPG le plus 61ev6 chez 59 moutons (48.4%). Parmi les 122 6chantillons examin6s, 84% contenaient 5 A 8 esp~ces de coccidies. Toutes les esp~ces sont d6crites pour la premiere fois au Zimbabwe.
257
Prevalence of coccidia in sheep in Zimbabwe R.C. Chhabra and V.S. Pandey Department of Paraclinical Veterinary Studies, University of Zimbabwe, Mount Pleasant, Harare. Zimbabwe (Accepted 24 September 1991 )
ABSTRACT Chhabra, R.C. and Pandey, V.S., 1992. Prevalence of coccidia in sheep in Zimbabwe. Small Rumin. Res., 8: 257-264. A total of 497 domestic sheep faecal samples, from three farms in Zimbabwe, were collected per rectum between February 1989 and March 1990 to survey intestinal coccidia. Number of oocysts per gram (OPG) of faeces was determined by the standard McMaster technique and identification of oocysts was done on sporulation. On average, 83.3% (range 72.8-92.8%) of samples were positive for coccidia oocysts. Among the positives, OPG was < 1000 in 71% of samples, 1500-5000 in 22%, 500010 000 in 3.6%, and above 10 000 in 3.4% of samples. The highest recorded OPG was 118 800. Animals showing counts over 10 000 OPG revealed a significant drop when examined after a month. Eleven species ofcoccidia were identified from 122 individual samples. Eimeria ovinoidalis ( =E. ninakohlyakimovae) was the most prevalent species, found in all animals, followed by E. parva (98.3%), E. ovina (95.0%), E. ahsata (91.0%), E. crandallis (69.7%), E. faurei (61.4%), E. granulosa (53.2%), E. caprovina (26.2%), E. pallida (24.6%), E. intrictata (23.8%) and E. christenseni (12.3%). E. ovinoidalis was the most predominant species, showing the highest counts in 59 sheep (48.4%). Of the 122 samples, 84% had five to eight species ofcoccidia. All species are reported for the first time from Zimbabwe.
INTRODUCTION
Eimeria species of coccidia are ubiquitous parasites occuring in many species of domestic animals, including sheep. A high prevalence of mixed infections by a number of Eimeria species has been reported in sheep from many countries (McKenna, 1972; Pout, 1973; Mason, 1977; Vercruysse, 1982; Gregory and Catchpole, 1987; Pandit et al., 1987; Manzhos et al., 1988 ). Eimeria species of sheep and goats shown earlier as identical are now considered as separate species on the basis of host-specificity experiments in these animals (McDougald, 1979; Sayin et al., 1980) and reviewed by Norton ( 1986 ). Coccidiosis caused by Eimeria species in sheep is an important intestinal condiCorrespondence to: V.S. Pandey, Institute of Tropical Medicine, Department of Tropical Animal Production and Health, Nationalestraat, 155, B-2000 Antwerp 1, Belgium.
258
R.C. CHHABRA AND V.S. PANDEY
tion, outbreaks in lambs causing high morbidity and mortality (Salisbury et al., 1953; Rusev, 1987; Manzhos et al., 1988). As there was no information available on coccidia of sheep in Zimbabwe and the relevance of work done in other countries to Zimbabwean conditions is doubtful, the present study was carried out to study the prevalence and intensity of coccidia in sheep in Zimbabwe. MATERIALS AND METHODS
Study sites The study was carried out in sheep at three farms, two within 20 km of Harare, namely 'U.Z.' and 'Siddiqui' and one at Makoholi, located about 250 km south of Harare. The climate of Harare is generally moderate with a warm, wet period from November to April and a mean annual rainfall of 800 m m , a cool dry period from May to August, and a hot, dry period from September to October/November. M a x i m u m mean monthly temperature of 29 ° C is recorded in October and m i n i m u m mean monthly temperature of 6.5 °C in July. The climate of Makoholi is drier than that of Harare, with a mean annual rainfall of 650 mm.
Animals The sheep were of the indigenous breed with some at Makoholi being crosses of indigenous × Merino. Each flock was run as a unit and grazed natural pastures with supplements during the dry season. Animals did not receive anticoccidial drugs during the study period. The age of the animals was from 4 months to adult. To determine the earliest natural infection with coccidia, six lambs separated from their coccidia-infected mothers 24-48 h after birth were maintained in cages under coccidia-free conditions and their faeces examined at 1- or 2-day intervals.
Faecal examination Faecal samples were collected per rectum in plastic bags from February 1989 to March 1990, and kept in a refrigerator at 4 °C until processed. A total of 497 faecal samples were examined. N u m b e r of oocysts per gram ( O P G ) of faeces was determined by the standard McMaster technique (Soulsby, 1982 ) to an accuracy of 1 oocyst counted, representing 50 oocysts per g of faeces.
Identification of species of coccidia Identification of Eimeria species was carried out on 122 individual faecal samples after sporulation in 2.5% potassium dichromate solution (McKenna, 1972 ). Oocysts were concentrated by centrifugal flotation using saturated sod i u m chloride solution (Soulsby, 1982 ). They were identified under a 40X, and at times a 100X objective. Usually 100 oocysts were identified from each
PREVALENCE OF COCCIDIA IN SHEEP IN ZIMBABWE
259
faecal sample. Measurements of oocysts were taken with a calibrated ocular micrometer under a 40X objective. For identification, various figures and descriptions given by earlier workers (Shah, 1963; Joyner et al., 1966; Pellerdy, 1974; Levine, 1985; Norton, 1986) were used, although at times it was subjective. RESULTS
Between 72.8 and 92.9% of samples examined were positive for Eimeria oocysts (Table 1 ). Over two-thirds of infected sheep had OPG less than 1000, and only 0.7% had over 50 000. Mean oocyst counts varied from 1256 to 1768, and the maximum recorded OPG was 118 800 (Table 2 ). There was no difference between the prevalence of coccidia of indigenous and crossbred sheep, but intensity of infection was higher in crossbred sheep. There appeared to be no important seasonal variation in oocyst counts. There was, however, marked fluctuation in oocyst counts of individuals examined at monthly intervals. A significant drop in TABLE 1 Prevalence of coccidia oocysts in faecal samples from sheep at three farms in Zimbabwe Farm
Number examined
Number positive (% positive )
Makoholi Siddiqui U.Z.
213 116 168
155 (72.8) 103 (88.8) 156 (92.9)
Total
497
414 (83.3)
TABLE2
Eimeriaoocystspergram(OPG) of~ecesinsheepatthree~rmsinZimbabwe RangeofOPG
50-950 1000-4950 5000-9950 10 000-49 950 50 000-99 950 Over 100 000 Mean OPG of all samples Max. OPG recorded
Percentage of infected sheep Makoholi
Siddiqui
76.8 20.6 0.7 0.7 0.6 0.6 1256 118 800
70.9 20.4 2.9 5.8 -
-
1768 48 600
Total
U.Z. 65.4 24.4 7.0 2.6 0.6 -
1293 29 000
71.0 22.0 3.6 2.7 0.5 0.2 1480 -
260
R.C. CHHABRAAND V.S.PANDEY
count was registered in animals showing OPG over l 0 000, and at times no oocysts were found in faeces of an individual re-examined after a month. A total of 11 species of Eimeria were identified. Percentages of animals harbouring different species are shown in Table 3. All samples had mixed infections with 3-10 species, and over 50% had 6-7 species (Table 4). E. ovinoidalis ( = E. n inakohlyakimovae) was the most predominant species, with highest counts in 48.4% of 122 sheep, followed by E. parva in 20.5%, E. ahsata in 12.3% and E. ovina in 8.2% of sheep (Table 5). Two species, E. crandallis TABLE 3 Prevalence rate (no. positive/no, examined× 100) of Eimeria species in sheep at three farms in Zimbabwe Eimeria species
Prevalence rate (%)
Makoholi
E. ovinoidalis E. parva E. ovina E. ahsata E. crandallis E. faurei E. granulosa E. caprovina E. pallida E. intricata E. christenseni
Siddiqui ( n = 14)
U.Z. (n=49)
Total
( n = 59) 1O0 98 95 98 73 56 56 22 29 19 19
I O0 93 93 93 100 43 43 57 0 28 14
1O0 100 96 82 57 73 53 22 27 29 4
1O0 98 95 91 70 61 53 26 25 24 12
( n = 122)
TABLE 4 Number o f Eimeria species in mixed infections in sheep at three farms in Zimbabwe Number o f Eimeria species
Three Four Five Six Seven
Eight Nine Ten
Percentage of samples infected Makoholi (n=59)
Siddiqui ( n = 14)
U.Z. (n=49)
Total
0 3.4 13.6 25.4 28.8 16.9 10.2 1.7
0 0 7.1 50.0 7.1 21.5 14.0 0
4.1 6.1 16.3 24.5 26.5 14.3 6.2 2.0
1.6 4.0 14.0 28.0 25.4 16.4 9.0 1.6
( n = 122)
PREVALENCE OF COCCIDIA IN SHEEP IN ZIMBABWE
261
TABLE 5 P r e d o m i n a n t E i m e r i a species in sheep at three f a r m s in Z i m b a b w e E i m e r m species
E. ovinoidalis E. parva E. ovina E. ahsata E.faurei E. granulosa E. caprovina E. pallida E. intricata
P r e d o m i n a n c e rate (%) Makoholi (n=59)
Siddiqui ( n = 14)
U.Z, (n=49)
Total ( n = 122)
40.6 32.2 3.4 15.3 6.8 1.7
50.0 7.1 14.3 14.3 7.1 7.1
57.1 10.2 12.2 8.2 2.0 4.1 4.1 2.0
48.4 20.5 8.2 12.3 0.8 4.9 0.8 1.6 2.5
and E. christenseni, did not have highest counts in any of the 122 samples examined. In the six lambs separated from their mothers 24-48 h after birth, Eimeria oocysts were detected for the first time when they were 18-28 days old. DISCUSSION
Prevalence of infection in sheep in the present study (Table 1 ) was similar to the infection rates of up to 95% recorded in other countries (Michael and Probert, 1970; McKenna, 1972; Catchpole et al., 1975; Vercruysse, 1982), but higher than the 69% recorded in Illinois, U.S.A. by Shah ( 1963 ). Although the majority of animals had oocyst counts below 1000 and the mean count of the three farms was 1480, a small proportion of sheep had very high counts (Table 2), and it is mainly these animals which contributed to heavy contamination of the environment. A similar phenomenon, that a few animals in an infected flock produce a large number of eggs, is known to occur in trichostrongylid nematodes of sheep (Windon, 1990 ). As reported by Pout and Ostler ( 1966 ) and Mason ( 1977 ), the present study also revealed marked fluctuation in faecal oocyst count of individuals examined at monthly intervals. Gregory and Catchpole (1987 ) claimed that oocyst counts done three days apart could be quite unrelated in numbers, heavily infected animals showing a drop in OPG when examined a month later. Similar observations were made in goats from the same areas of Zimbabwe (Chhabra and Pandey, 1991 ). According to Davies et al. ( 1963 ) and Mason ( 1977 ), with increasing infective dose of oocysts a point is reached where inhibition of oocysts occurs, resulting in decreased faecal oocyst output. However, the fluctuation in oocyst
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R.C. CHHABRA AND V.S. P A N D E r
output may be due to local immune response (Barriga, 1981 ), circadian rhythm, and age (Pout, 1973; Mason, 1977). Crossbreds of indigenous × Merino sheep had a higher intensity of infection, as was the case with coccidial infection of crossbred goats from the same locality (Chhabra and Pandey, 1991 ). E. ovinoidalis, E. parva, E. ovina ( = E. arloingi ) and E. ahsata, which were present in 90-100% of sheep with high predominance (Tables 3 and 5 ), are reported to be very pathogenic and may cause overt coccidiosis (Lotze, 1954; Smith et al., 1960; Horton and Stockdale, 1979; Manzhos et al., 1988; Gregory et al., 1989 ). Mixed infection with several species of coccidia (Table 4) is the rule in natural infections, although the number and composition of species may vary (Michael and Probert, 1970; Mason, 1977). The first appearance ofoocysts at the age of 18-28 days in lambs separated from their mothers 24-48 h after birth and thereafter kept in coccidia free conditions, supports the view that lambs can pick up infectionjust after birth, probably from their mother's udder or body, and become patent in the first 3-5 weeks of life (Pout and Ostler, 1966; Mason, 1977). In conclusion, it may be stated that the prevalence of coccidia in sheep in Zimbabwe is high. Out of 11 species reported, the prevalence and predominance of known pathogenic species is high and coccidiosis as a disease entity in sheep in Zimbabwe merits further investigation. ACKNOWLEDGEMENTS
Thanks are due to the technical staff of the Parasitology Laboratory of the Department of Paraclinical Veterinary Studies for their able assistance, to the different farms for the collection of samples, and for the grant provided by the Research Board, University of Zimbabwe, to carry out this work. REFERENCES Barriga, O.O., 1981. The immunology of parasitic infections. A Handbook for Physicians, Veterinarians and Biologists. University Park Press, Baltimore, 354 pp. Catchpole, J., Norton, C.C. and Joyner, L.P., 1975. The occurrence of Eimeria weybridgensis and other species of coccidia in lambs in England and Wales. Br. Vet. J., 131:392-401. Chhabra, R.C. and Pandey, V.S., 1991. Coccidia of goats in Zimbabwe. Vet. Parasitol., 39:199205. Davies, S.M.F., Joyner, L.P. and Kendall, S.B., 1963. Coccidiosis. Oliver and Boyd, London, 264 pp. Gregory, M.W. and Catchpole, J., 1987. Output of coccidial oocysts (particularly Eirneria crandallis) by naturally infected lambs: daily and hourly patterns and clinical significance. Dtsch. Tier~irztl. Wochenschr., 94:521-525. Gregory, M.W., Catchpole, J., Nohan, A. and Herbert, C.N., 1989. Ovine coccidiosis: studies on the pathogenicity of Eimeria ovinoidalis and E. crandallis in conventionally-reared lambs, including possible effects of passive immunity. Dtsch. Tier~irztl. Wochenschr., 96: 287-292.
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Horton, G.M.J. and Stockdale, P.H.G., 1979. Effects of amprolium and monensin on oocyst discharge, feed utilization, and ruminal metabolism of lambs with coccidiosis. Am. J. Vet. Res., 40: 966-970. Joyner, L.P., Norton, C.C., Davies, S.F.M. and Watkins, C.V., 1966. The species of coccidia occurring in cattle and sheep in the South-West of England. Parasitology, 56:531-541. Levine, N.D., 1985. Veterinary Protozoology. 1st Edn. Iowa State University Press, Ames, IA, 414pp. Lotze, J.C., 1954. The pathogenicity of the coccidian parasite, Eimeria ninakohlyakimovae (Yakinov and Rastegaieff, 1930 ) in domestic sheep. Proc. Am. Vet. Med. Assoc., 1953:141 146.
Manzhos, A.F., Prikhod'ko, Yu.A., Sumtsov, V.S. and Kolomatskii, A.P., 1988. Eimeria infection in sheep: epidemiology, diagnosis and economic losses. Veterinariya, Moscow, 7: 3437. Mason, P., 1977. Naturally acquired coccidia infection in lambs in Otago. N. Z. Vet. J., 25: 3033. McDougald, L.R., 1979. Attempted cross-transmission of coccidia between sheep and goats and description of Eimeria ovinoidalis (sp.n.). J. Protozool., 26:109-113. McKenna, P.B., 1972. The identity and prevalence of coccidia species in sheep and cattle in New Zealand. N. Z. Vet. J., 20: 225-228. Michael, E. and Probert, J., 1970. The prevalence of coccidia in faecal samples from sheep in North Wales. Res. Vet. Sci., 11: 402-405. Norton, C.C., 1986. Coccidia of the domestic goat Capra hircus, with notes on Eimeria ovinoidalis and E. bakuensis (syn. E. ovina) from the sheep Ovis aries. Parasitology, 92: 279-289. Pandit, B.A., Prasad, K.D. and Sahai, B.N., 1987. Prevalence of Eimeria infections in sheep of Chotanagpur, Bihar. J. Vet. Parasitol., 1:71-75. Pellerdy, L.P., 1974. Coccidia and Coccidiosis. 2nd Edn. Paul Parey, Berlin, 959 pp. Pout, D.D., 1973. Coccidiosis of lambs: 1. Observations on the naturally acquired infection. Br. Vet. J., 129: 555-567. Pout, D.D. and Ostler, D.C., 1966. The coccidial population in clinically normal sheep. Vet. Rec., 78: 455-460. Rusev, I., 1987. Treatment and prophylaxis of coccidiosis in lambs and kids. Veterinarna Sbirka, 85: 17-18. Salisbury, R.M., Muir, J. and Stifling, J., 1953. Coccidiosis as a probable cause of unthriftiness and deaths in lambs. N. Z. Vet. J., 1: 72-77. Sayin, F., Dincer, S. and Milli, U., 1980. The life cycle and pathogenicity of Eimeria arloingi (Marotel, 1905) Martin, 1909 in Angora kids and an attempt at its transmission to lambs. Zentralbl. Vet. Med., Reihe B., 27: 382-397. Shah, H.L., 1963. Coccidia (Protozoa: Eimeriidae) of the domestic sheep in the United States, with descriptions of the sporulated oocysts of six species. J. Parasitol., 49: 799-807. Smith, W.N., Davies, L.R. and Bowman, G.W., 1960. The pathogenicity of Eimeria ashata, a coccidium of sheep. J. Protozool., 7: Suppl., 8. Soulsby, E.J.L., 1982. Helminths, Arthropods and Protozoa of Domesticated Animals. 7th Edn., Bailliere Tindall, London, 809 pp. Vercruysse, J., 1982. The coccidia of sheep and goats in Senegal. Vet. Parasitol., 10: 297-306. Windon, R.G., 1990. Selective breeding for the control ofnematodiasis in sheep. Rev. Sci. Tech. Off. Int. Epiz., 9: 555-576. RESUME Chhabra, R.G. et Pandey, V.S., 1992. Pr6valence de la coccidie chez les moutons au Zimbabwe. SmalI Rurnin. Res., 8: 257-264.
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De f6vrier 1989 h mars 1990, 497 6chantillons de mati~res f6cales, r6colt6s directement au niveau du rectum de moutons provenant de trois fermes au Zimbabwe, ont 6t~ examin6s pour la recherche des coccidies intestinales. Le nombre de oocysts par g de f~ces (OPG) 6tait 6valu6 par la technique classique de McMaster, et les oocysts ont 6t6 identifi6s apr~s leur sporulation. En moyenne 83.3% (extremes 72.8-92.8%) des 6chantillons 6taient positifs pour la coccidioses. Parmi les 6chantillons positifs, 71% avaient un OPG de moins de 1000, 3.6% de 1500 h 5000 et 3.4% de plus de 10 000. L'OPG le plus 61ev6 6tait de 118 800. Les animaux avec un OPG de plus de 10 000 examin6s un mois plus tard, ont montr~ une diminution significative du nombre d'oocysts dans leur f~ces. Un examen de 122 6chantillons individuels a permis l'identification de 11 esp~ces diff6rentes de coccidies. Eimeria ovinoidalis ( =E. ninakohlyakirnovae) 6tait l'esp~ce la plus fr6quente et fur rencontr6e dans 100% des 6chantillons. Elle 6tait suivie de E. parva (98.3%), E. ovina (95.0%), E. ahsata (91.0%), E. crandallis (69.7%), E. faurei (61.4%), E. granulosa (53.2%), E. caprovina (26.2%), E. pallida (24.6%), E. intricata (23.8%) et E. christenseni (12.3%). E. ovinoidalis 6tait l'esp~ce la plus dominante, avec I'OPG le plus 61ev6 chez 59 moutons (48.4%). Parmi les 122 6chantillons examin6s, 84% contenaient 5 A 8 esp~ces de coccidies. Toutes les esp~ces sont d6crites pour la premiere fois au Zimbabwe.