Trop, Anita. Hlth Prod. (1979) 11,151-156

OVINE FASCIOLIASIS (FASCIOLA GIGANTICA) ON THE AHMADU BELLO UNIVERSITY FARM T. W . SCHILLHORN VAN VEEN

Faculty of Veterinary Medicine, Ahmadu Bello Veterinary, Zaria SUMMARY

Outbreaks offascioliasis (Fasciola gigantica) in sheep were observed on the Ahmadu Bello University farm during the end of the dry season in 1972-74 and in 1978. During 1972 especially the pregnant ewes were affected. Pre- and post-mortem examination of the affected sheep showed typical signs of acute fascioliasis; the number of flukes in the liver ranged between 77 and 239. The infections were acquired when the animals grazed near the man-made lake on the farm. A limited snail survey revealed the presence of Lymnaea natalensis with the highest incidence of snails as well as of larval Fasciola infections in the snails during the beginning of the dry season. There was an indication that the control measures taken after 1974, i.e. not allowing the animals to graze around the lake especially during the wet season, prevented the occurrence of outbreaks in 1975-77.

INTRODUCTION

Fasciola gigantica is commonly observed in ruminants in the northern states of Nigeria. The infections are acquired in temporarily flooded areas like the floodplains of the Niger and Benue rivers as well as of the smaller rivers and streams in the Guinea and Sudan vegetational zone (Ferguson, 1964). Fascioliasis is mainly observed in the chronic form, either in young animals during the rainy season due to recently acquired infections, or in the dry season in older animals which, at that time, are in a poor condition and not well able to resist the effect of a relatively small number of flukes (Graber, 1971). In Nigeria, acute liver fluke infections are rarely seen in cattle but have been reported in small ruminants (Henderson, 1937). The present development in tropical agriculture, especially in arid areas, is often accompanied by changes in water management (dams, dikes, and irrigation) and a subsequent increase in the number of biotypes suitable for development and survival of aquatic snails. The danger of this change in water management and increase in snail habitats is well-known in relation to human trematode infections but is, in West Africa, less frequently considered in relation to snail-borne diseases like fascioliasis in domestic animals. In this communication, some epidemiological aspects of outbreaks of acute fascioliasis in sheep grazing near an artificial lake during 1972 to 1978 are considered.

MATERIALS AND METHODS

The University farm is located in the northern Guinea savanna vegetational zone at approximately 16 km from Zaria. In 1967 a dam was constructed in a small perennial stream creating a lake which at its highest level covered an area of approximately Present address: Veterinary Clinical Center, Michigan State University,East Lansing, Michigan 48824, USA. 151

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15 ha. The take was fairly shallow and at its lowest level, during the drought of 1973 to 1974, it covered little more than 1 ha. The water level showed seasonal fluctuations with the highest level during the beginning of the dry season (October). The level dropped gradually during the dry season due to evaporation, drinking by animals and to the offtake of water for some small irrigation plots. The lowest level was reached just before the beginning of the rains in April or May. The climate in the Zaria area is characterised by a rainy season from May to October and a dry season from November to April. The rainfall during the period November to March is nil and the humidity during the dry season is often below 20~o. The length of the rainy season and consequently of the dry period varies considerably; the dry season in 1972 to 1973 lasted nearly 8 months compared to only 5 months in 1975 to 1976 (Fig. 1). A PR

1971 1972 1973 1974

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FIG. 1. Duration of the rainy season during 1972-1978. A mixed herd of about 100 White Fulani cattle and 100 to 150 Yankassa sheep was grazing freely on the farm supervised by a herdsman. At night the animals were penned up. In the beginning of the dry season the animals were mainly grazing crop residues (sorghum, maize). Later in the dry season they moved into the small dried-up floodplain around the lake. RESULTS

Case history

The first casualties due to acute fascioliasis in the sheep flock were observed in June 1972, At that time, no drugs acting against immature flukes were available and the animals were treated with hexachlorethane. 1 Seven animals died in June and one in July. In 1973 another outbreak of acute fascioliasis occurred at the end of April and 4 animals died. The rest of the flock was treated with menichlopolan z and no further casualties were observed. At the end of February 1974 an outbreak of acute paramphistomiasis (Paramphistomum microbothrium) occurred in the sheep flock. Postmortem examination of the fatal cases revealed, besides the intestinal lesions due to juvenile paramphistomes, some very small (2 to 7 ram) immature F. giganticain the liver parenchyma. The number of young flukes per liver ranged between 2 and 61 (Table I). The surviving animals 1Avlothane (tCI) 200 mg/kg.

= Bilevon-M(Bayer). 5-7 mg/kg.

OVINE FASCIOLIASISIN NIGERIA

153

TABLE] Number and size (mm) of F. gigantica recovered from sheep in the University farm Animal number 996(p) 786(p) 727(p) 214(p) 1966 91 801 109 720B 29M 989N(p) 1898N 1874M 137M 119B(p)

Date of death 16.6.72 17.6.72 24.6.72 20.7.72 20.2.74 20.2.74 20.2.74 20.2.74 4.4.74 4.4.74 8.4.74 6.4.74 6.4.74 6.4.74 6.4.74

Cause of death Fascioliasis Fascioliasis Fascioliasis Fascioliasis Paramphistomiasis Paramphistomiasis Paramphistomiasis Paramphistomiasis Fascioliasis Fascioliasis Faseioliasis Slaughtered Slaughtered Slaughtered Slaughtered

Number of flukes

Size of flukes

Liver Lung Other

Mean

156 171 131 77 6I 16 2 30 124 226 224 239 33 98 43

4 6 6 1 0 0 0 0 0 0 3 0 0 0 0

0 3t 0 22 0 0 0 0 0 0 0 0 0 0 0

20 20 21 28 4 4 4 7 25 27 30 !6 21 17 22

Range 12-25 13-25 15-30 18-32 2~z-5 2~-7 3-5 4-9 20-30 18-30 23-33 no data no data no data no data

Eggs observed 0 0 0 yes 0 0 0 0 0 0 0 0 0 0 0

1 Flukes in pancreas; 2 flukes in kidney; p: pregnant; M: treated with menichlopholan; B: treated with bithionol; N: treated with nictosamide.

were divided into 3 groups which were treated respectively with menichlopholan, bithionol-sulphoxyde3 and niclosamide. 4 Two months later 5 animals died of acute fascioliasis, one each from menichlopholan- and bithionol-treated groups and 3 animals which had been treated with niclosamide. Some animals which were slaughtered for other reasons also showed flukes in their livers. The number o f flukes found in the liver-parenchyma o f the 7 animals examined ranged between 33 and 239 (Table I). After 1974, the farm manager was advised to cut the grass in the floodplains and change the grazing pattern of the herd in such a way that the animals were not allowed to graze along the lake during the wet season and as little as possible during the dry season. (It was not possible to prevent all grazing near the lake as little alternative pasture was available at the end o f the dry season.) Casualties due to fascioliasis were not observed during 1975, 1976 and 1977. Then grazing control was released and in 1978, two sheep died of acute fascioliasis during the middle of April.

Clinical observations Most animals died suddenly without marked clinical signs before death though some were unthrifty and most animals showed some degree of anaemia. The surviving animals also showed little evidence of liverfluke infections and their packed cellvolumes varied between 23 and 35 %. In 1972 all casualties were pregnant females in the second month of pregnancy. In 1973 and 1974 only 2 of the fatal cases were pregnant ewes, although all were adult female sheep. The cattle grazing with the sheep, a Disto-5 (Cogla) 35-50 mg/kg. 4 Mansonil (Bayer) 100-125 mg/kg.

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although infected, showed no clinical evidence of fascioliasis. These animals were routinely treated with flukicides between February and April each year.

Pathology After routine necropsy, the liver was removed, sliced, and the flukes removed and counted. Other organs were closely examined for evidence of flukes. In certain cases the flukes were measured after having been left overnight in physiological saline at 4°C. In June 1972 representative tissue samples were collected, fixed in buffered formalin and stained in haematoxin/eosin and, occasionally, in toluidineblue. Post-mortem examination of the sheep which died in 1972 showed pale animals with an abdominal cavity filled with blood-tinged fluid. The liver capsule, especially the abdominal aspect, was covered with a fibrinous gelatinous coat with adhesions to other organs in the body cavity. The gross appearance of the infected livers was similar to that reported in acute fascioliasis due to F. hepatica. Young flukes were found throughout the liver parenchyma and sometimes in the bile ducts. The liver was enlarged, congested, and friable. The capsule showed numerous punctures with young F. gigantica protruding. A few flukes were found in the body cavity, in the lungs and pancreas and, only once, in the kidney (Table I). Apart from paramphistomes and a few Dicrocoelium sp. in one sheep, concurrent trematode infections were not detected. The foetuses of the ewes which had succumbed did not shown any gross evidence of fluke infection.

Snail sampling Snail sampling started in 1973 and continued to 1975. Snails were collected by handpicking from different sites along the lake. The number of snails collected in 5 min was used as the quantitative criteria. In the laboratory the snails were crushed and examined for evidence of larval Fasciola infections. The major snail species found were Lymnaea natalensis, Bulinus globosus and Biomphalaria pfeifferi. Most snails were found during the beginning of the dry season especially in 1974. A low number of Lymnaea was found in the wet season and in September and October 1973 but that was probably biased as the dense vegetation at that time often hindered the sampling. No snails were found in April to June during the 5 rain search. Faseiola infected snails were only detected in the period October to February in both years. DISCUSSION

The clinical and pathological changes appeared more or less similar to those reported in acute fascioliasis due to F. hepatica (Ross and Dew, 1967; Rushton and Murray, 1977). The number of flukes causing the damage was, however, smaller. Also, Katiyar and Tewari (1962) reported similar findings and fluke numbers between 128 and 198. It should be realised, however, that the average weight of the affected Yankassa sheep ranged between 25 and 35 kg; their livers weighed between 300 and 700 g. The outbreaks occurred in the second half of the dry season and, apart from the first outbreak in 1972, all in April. The 1972 outbreak was an exception and it only occurred in pregnant ewes which may have shown a different grazing behaviour as well as a different immunological status. The niclosamide treated sheep carried the highest number of flukes. This was to be

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155

expected as niclosamide has little effect against Fasciola spp. The low efficacy of the other 2 drugs is probably due to a too early treatment in February. At that time, the young flukes measuring 2 to 7 mm were approximately 4 to 6 weeks old (Hanna, 1976) and the efficacy of bithionol as well as of menichlopholan against flukes less than 6 weeks old is medibcre (Hildebrandt, 1968; Berger, 1971). It appears then that simultaneous (one-shot) treatment against juvenile paramphistomes and liverflukes is not feasible with the drugs used. Treatment later in March would probably have prevented the outbreaks of fascioliasis. The change in grazing management, however, seemed an easier and cheaper control method but needs strict adherence. Assuming a pre-patent period of approximately 3 months indicates that the infections in 1973, 1974 and 1978 were acquired during January and February. This is more or less confirmed by the size and age, according to Hanna's data (1976), of the immature flukes recovered at the end of February 1974 from the sheep which died of paramphistomiasis. It is also in accordance with the little available information on the infection pattern in the snail intermediate hosts. The total Lymnaea population, as measured by the rather rough method of handpicking for a fixed period, was reduced in 1972 to 1973 and 1973 to 1974 when compared to the wetter year 1974 and 1975. Despite this smaller snail population, some animals apparently acquired a fairly high number of metacercariae--at least sufficient to cause disease. This is likely to be associated with the low level of the lake and the smaller size of the floodplain during those years causing a more concentrated distribution of metacercariae on the grass, as well as more intensive grazing by the animals. Most work on ovine fascioliasis has been done in animals grazing in fenced pastures with a limited botanical composition and with European breeds of sheep. The freerange grazing of these Yankassa sheep in the University farm, however, presented a more varied botanical diet. Moreover, Nigerian sheep are more browsing than European breeds (W. Brinckman, personal communication) and could be more selective grazers. Pregnant ewes, however, may be less selective during pregnancy and might under such conditions use parts of the pasture which normally would not be grazed. ACKNOWLEDGEMENTS

The co-operation of the staff of the University farm, of Dr D. Shannon, the attending veterinarian, of Drs Barnes and Bida from the Veterinary Pathology Department and of Messrs S. Usman and T. Ishaya of the Helminthology Section is gratefully acknowledged. This study was supported in part by a grant from the Netherlands Foundation for Advancement of Tropical Research. Accepted for publication March 1979 REFERENCES BERGER, J. (1971). Bulletin of Epizootic Diseases of Africa, 19, 37-44. FI~RGUSON,W. (1964). Bulletin of Epizootic Diseases of Africa, 12, 331-334. G~BER, M. (1971). Bulletin of Epizootic Diseases of Africa, 19, 45-60. HANNA, R. E. B. (1976). Research in Veterinary Science, 21,244-246. H~NDERSON,W. W. (1937). Annual Report of the Veterinary Department, Nigeria, 1935, 15. HILDEBI~NDT, J. (1968). Berliner und Miinchener Tieriirtzlichen Wochenschrift, 81, 66--69. I~TIYAR, R. D. & T~WAnI, H. C. (1962). Indian Veterinary Journal, 39, 382-386. Ross, J. B. & Dow, C. (1967). The Veterinary Record, 80, 543. RUSHTON, B. & MURRAY,M. (I 977). Journal of Comparative Pathology, 87, 459-470.

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LA FASCIOLOSE OVINE (FASCIOLA GIGANTICA) A LA F E R M E D E L ' U N I V E R S I T E A H M A D U BELLO R~sum~--Des foyers de fascioiose (Fasciolagigantica) ovine ont ~t~ observ~ ~t la ferme de l'Universit6 Ahmadu Bello durant la fin de la saison s ~ h e en 1972 et 1974 et en 1978. En 1972, ce sont surtout les brebis gestantes qui,ont 6t6 touehe~s. L'examen ante et post-mortem des sujets atteints a montr6 qu'il s'agissait de fasciolose aigu~, le hombre des douves d ~ o m p t ~ ' s dans les roles allant de 7 7 / t 239. Les animaux se sont infest.~ en phturant pros d'un lae artificiel creus~ clans la ferm¢ m~me. Une enqu~te l i m i t ~ sur les mollusques presents a r~v~16 la pr~senee de Lymnaea natalensis en plus grand nombre et infect~es de larves de Fasciola au d~but de la saison s ~ h e . I1 est indiqu6 qu'~t la suite des mesures prises apr~s 1974, consistant/t interdire aux animaux de p~turer aux abords du iae Sl~cialement durant la saison des pluies, rapparition de foyers en 1977 et 1977 a ~t~ ~vit~e. FASCIOLASIS OVINA (FASCIOLA GIGANTICA) EN LA G R A N J A U N I V E R S I T A R I A A H M A D U BELLO Resumen---Se estudiaron brotes de faseiolasis (Fasciola gigantica) en ovejas de la granja universitaria Ahmadu Bello, al final de la estaci6n seca en 1972-1974 y 1978. En los brotes oeurridos en 1972, la mayoria de casos se presentaron en ovejas gestantes. El examen ante y postmortem de los animales afectados, revel6 lesiones tlpicas de fasciolasis aguda; el nt~mero de par~isitos en el higado fluctu6 entre 77 y 239. Los animales s¢ infectaron cuando pastorearon cerca del lago de la Granja. U n 6'studio limitado de caracoles, revel6 la presencia de Lymnaea natalensis con la incidencia m ~ alta de caracoles e infeeeiones de estos con larvas de Fasciola, al principio de ia estaci6n seca. Las medidas preventivas tomadas despues de 1974, consistentes ¢n impedir que los animales pastorearan cerca d¢l lago durant¢ la estaci6n Iluviosa, fueron efectivas durante 1975-77.