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Haemonchus contortus with low inhibited development in sheep from the highveld of Zimbabwe
Veterinary Parasitology, 36 (1990) 347-351 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
347
Short Communication
Haemonchus
c o n t o r t u s with Low Inhibited
D e v e l o p m e n t in Sheep from the Highveld of Zimbabwe V.S. PANDEY
Department of Paraclinical Veterinary Studies, Faculty o[ Veterinary Science, University of Zimbabwe, P.O. Box MP 167, Mount Pleasant, Harare (Zimbabwe) (Accepted for publication 20 December 1989)
ABSTRACT Pandey, V.S., 1990. Haemonchus contortus with low inhibited development in sheep from the highveld of Zimbabwe. Vet. Parasitol., 36: 347-351. The abomasa of sheep grazing on natural pastures in the highveld of Zimbabwe were examined for Haemonchus contortus. Of 304 abomasa, 213 (70%) barboured H. contortus. The worm burden increased during the rains to reach the peak in February-March. This was followed by a decline with low worm loads throughout the dry season. The fourth stage larvae (L4) accounted for 1-7 % of the total H. contortus population, except during July and August when they comprised 22 and 54% of the worm burden, respectively. It appears that the inhibition of H. contortus is not common in the commercial farming sector where sheep are treated very frequently.
INTRODUCTION
In Zimbabwe, like many other countries, Haemonchus contortus is considered to be the most important nematode in sheep (Grant, 1981) and goats (Jansen and Pandey, 1989). However, very little information is available on its epidemiology. Grant (1981) conducted a study on an experimental farm where no anthelmintics were given to lambs during a 1-year trial period. In practice, sheep are treated frequently with anthelmintics, the most common being albendazole, oxfendazole, rafoxanide and levamisole. Therefore it is possible that the pattern of infection in natural conditions may be different from the experimental situation. The inhibition of development or hypobiosis of trichostrongylids, including H. contortus, in the northern hemisphere is common and is believed to be due to the falling temperatures or chilling (Gibbs, 1982). In tropical areas, reports on the occurrence of hypobiosis of H. contortus are conflicting (Allonby and 0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
348
v.s. PANDEY
Urquhart, 1975; Vercruysse, 1984; Chiejina et al., 1988) and, although the exact cause is not known, it is believed to be because of the dry conditions. The purpose of the present work was to study the seasonal variation in the worm burden of H. contortus of sheep under the normal field management conditions in the high rainfall area of Zimbabwe. M A T E R I A L S AND M E T H O D S
The study was carried out on sheep slaughtered at Mt. H a m p d e n abattoir, situated ~ 20 km northwest of Harare ( 17 ° 50' S, 31 ° 0' E, 1471 m). This abattoir obtains sheep mainly from commercial farmers within a radius of 100 km. The climate of the area, known as highveld, is characterised by a warm rainy period from N o v e m b e r / D e c e m b e r to March/April with a mean annual rainfall of 800-900 mm. The rainy season is followed by a cool dry period from May to August and a hot dry period from September to October/November. The meteorological data from Harare are considered to be typical of the area of the study and were obtained from Zimbabwe meteorological Office, Harare. Weekly visits were made to the abattoir between October 1985 and September 1986. On each visit 4-9 abomasa of sheep were collected. The origin, sex and age was recorded for each animal. Of 304 animals examined, 212 were 612 months, 44 1-2 years, 20 2-3 years and 20 > 3 years old. The abomasum was slit open in the laboratory. The contents were emptied into a bucket and the mucosa was then washed with water into another bucket. The mucosa was scraped off and digested in H C l - p e p s i n solution overnight at 37 ° C. Either all or half of the samples of contents, washings and mucosal digesta were searched for helminths. RESULTS
Of the abomasa examined, 213 (70%) were found to be infected with H. contortus. The prevalence of infection varied from a minimum of 50% in
M a y to a maximum of 89% in March. The mean monthly worm burden and corresponding meteorological data are presented in Fig. 1. The number of worms increased from December to reach a peak during Febm a r y - M a r c h . This was followed by a sharp decline in April and the numbers remained at a relatively low level until September with certain fluctuations. In general, the number of worms was low between April and November. The proportion of fourth stage larvae (L4) was between 1 and 7% during all the months of the year, except in July and August when 22 and 54%, respectively, of worms were in the L4 stage.
H. CONTORTUS WITH LOW INHIBITEDDEVELOPMENT
349
600m 500. i4OO.
~
300
: 200:~ 1OO0
,
ON
i
i
0
J
i
i
i
,
,
i
,
F MAM
JJuAS
, , . F M AM
~ ~ ; JJuAS
i
200
, . . . . ON D J
~'
(.I o
4
20
-
-
~
-
: ~ . . ~ m a x .
_
:.. ,o 1.... ~
o, O N D J
FMAMJ
JuA$
Fig. 1. Mean monthly maximum and minimum temperature, rainfall and H. c o n t o r t u s burden of sheep.
DISCUSSION The overall prevalence of infection was lower than that recorded by Grant (1981). The worm counts showed a trend which was correlated to the rainfall (Fig. 1). The ideal conditions of rain and temperature would have favoured the development, translation and survival of infective larvae of H. contortus leading to a gradual increase in worm burden from December onwards. The peak burden recorded in February-March can be accounted for by these favourable environmental conditions. The rainfall diminished from March and there was no rainfall from May to September (Fig. 1 ). As the dry cool weather is not conducive to the development of free-living stages (Gordon, 1950 ), there is very little possibility of the acquisition of new infections during this period. This is reflected in a lower worm burden during this period. The proportion of L4 was low throughout the year. Similar results have been found in Kenya (Allonby and Urquhart, 1975), Nigerian savanna and Malaysia (Chiejina et al., 1988). It is possible that our technique for the recovery of
350
v.s. PANDEY
hypobiotic larvae was not sensitive enough and therefore their numbers are underestimated. The recovery of hypobiotic larvae of Ostertagia ostertagi from cattle by the incubation of abomasal mucosa in buffered saline for 24 h is three times higher than the HCl-pepsin digestion used in the present work (Gasbarre, 1987). In a study in Zimbabwe, Grant (1981) recorded 0-10% ofH. contortus as L4 from October to April and 38-72% from May to September. The results in the present study are different. The possible explanation for these differences may be either differences in management or in the weather conditions. The work of Grant (1981) was carried out on a research station where animals received no anthelmintics during the whole period of study. The animals in the present work came from commercial farms where anthelmintic administration is frequent, generally every 2-3 weeks during the rainy season and every 3-5 weeks during the dry season. This difference in anthelmintic treatment is manifested in a lower worm burden in the present work. The annual rainfall during the present period of study was 1036 mm compared with an average of 850 mm in normal years. During the period of study by Grant (1981), the annual rainfall was only 474 mm, a drought situation. It may be that frequent anthelmintic treatment does not allow inhibition of larvae of H. contortus. Alternatively, the very dry conditions during the period of study by Grant (1981), coupled with no anthelmintic medication, were conducive to the inhibition of larvae. Supporting evidence for low inhibition of strongyles comes from an epidemiological study of parasites of donkey from the highveld of Zimbabwe. Very few inhibited larvae of small strongyles were observed even during the dry period of the year (Eysker and Pandey, 1987, 1989). It appears that in the highveld of Zimbabwe, inhibition of strongyle larvae is not important. More controlled work needs to be done to clarify the importance of inhibited larvae in the epidemiology of H. contortus under management conditions of sheep in the highveld of Zimbabwe. This study demonstrates that infection with H. contortus is high during the warm rainy season despite intensive anthelmintic treatment. This seems to be due to the fact that animals are set stocked, often at a high stocking rate. If infection levels are to be reduced, the sheep should be moved to cleaner pastures after anthelmintic treatment. ACKNOWLEDGEMENTS Grateful thanks are due to M. Taruvinga and V. Bhariri for their able technical assistance, to J. Harvey, Manager of Mt. Hampden abattoir, for providing the facilities and to Rosemary Mubaiwa for typing the manuscript.
H. C O N T O R T U S WITH LOW I N H I B I T E D DEVELOPMENT
351
REFERENCES Allonby, E.W. and Urquhart, G.M., 1975. The epidemiology and pathogenic significance of haemonchosis in a Merino flock in East Africa. Vet. Parasitol., 1: 129-143. Chiejina, S.N., Fakae, B.B. and Eze, B.O., 1988. Arrested development of gastrointestinal trichostrongylids in goats in Nigeria. Vet. Parasitol., 28: 103-113. Eysker, M. and Pandey, V.S., 1987. Overwintering of non-migrating strongyles in donkeys in the highveld of Zimbabwe. Res. Vet. Sci., 42: 262-263. Eysker, M. and Pandey, V.S., 1989. Small strongyle infections in donkeys from the highveld of Zimbabwe. Vet. Parasitol., 30: 345-349. Gasbarre, L.C., 1987. Recovery of third-stage larvae of Ostertagia ostertagi from the abomasa of experimentally inoculated calves by prolonged saline incubation. Proc. Helminthol. Soc. Wash., 54: 160-161. Gibbs, H.C., 1982. Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Vet. Parasitol., 11: 25-48. Gordon, H.Mcl., 1950. Some aspects of parasitic gastro-enteritis of sheep. Aust. Vet. J., 26: 14-52, 93-98. Grant, J.L., 1981. The epizootiology of nematode parasites of sheep in a high-rainfall area of Zimbabwe. J. S. Afr. Vet. Assoc., 52: 33-37. Jansen, J. and Pandey, V.S., 1989. Observations on gastro-intestinal helminths of goats in Zimbabwe. Zimbabwe Vet. J., 20: 11-13. Vercruysse, J., 1985. The seasonal prevalence of inhibited development of Haemonchus contortus in sheep in Senegal. Vet. Parasitol., 17: 159-163.
347
Short Communication
Haemonchus
c o n t o r t u s with Low Inhibited
D e v e l o p m e n t in Sheep from the Highveld of Zimbabwe V.S. PANDEY
Department of Paraclinical Veterinary Studies, Faculty o[ Veterinary Science, University of Zimbabwe, P.O. Box MP 167, Mount Pleasant, Harare (Zimbabwe) (Accepted for publication 20 December 1989)
ABSTRACT Pandey, V.S., 1990. Haemonchus contortus with low inhibited development in sheep from the highveld of Zimbabwe. Vet. Parasitol., 36: 347-351. The abomasa of sheep grazing on natural pastures in the highveld of Zimbabwe were examined for Haemonchus contortus. Of 304 abomasa, 213 (70%) barboured H. contortus. The worm burden increased during the rains to reach the peak in February-March. This was followed by a decline with low worm loads throughout the dry season. The fourth stage larvae (L4) accounted for 1-7 % of the total H. contortus population, except during July and August when they comprised 22 and 54% of the worm burden, respectively. It appears that the inhibition of H. contortus is not common in the commercial farming sector where sheep are treated very frequently.
INTRODUCTION
In Zimbabwe, like many other countries, Haemonchus contortus is considered to be the most important nematode in sheep (Grant, 1981) and goats (Jansen and Pandey, 1989). However, very little information is available on its epidemiology. Grant (1981) conducted a study on an experimental farm where no anthelmintics were given to lambs during a 1-year trial period. In practice, sheep are treated frequently with anthelmintics, the most common being albendazole, oxfendazole, rafoxanide and levamisole. Therefore it is possible that the pattern of infection in natural conditions may be different from the experimental situation. The inhibition of development or hypobiosis of trichostrongylids, including H. contortus, in the northern hemisphere is common and is believed to be due to the falling temperatures or chilling (Gibbs, 1982). In tropical areas, reports on the occurrence of hypobiosis of H. contortus are conflicting (Allonby and 0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
348
v.s. PANDEY
Urquhart, 1975; Vercruysse, 1984; Chiejina et al., 1988) and, although the exact cause is not known, it is believed to be because of the dry conditions. The purpose of the present work was to study the seasonal variation in the worm burden of H. contortus of sheep under the normal field management conditions in the high rainfall area of Zimbabwe. M A T E R I A L S AND M E T H O D S
The study was carried out on sheep slaughtered at Mt. H a m p d e n abattoir, situated ~ 20 km northwest of Harare ( 17 ° 50' S, 31 ° 0' E, 1471 m). This abattoir obtains sheep mainly from commercial farmers within a radius of 100 km. The climate of the area, known as highveld, is characterised by a warm rainy period from N o v e m b e r / D e c e m b e r to March/April with a mean annual rainfall of 800-900 mm. The rainy season is followed by a cool dry period from May to August and a hot dry period from September to October/November. The meteorological data from Harare are considered to be typical of the area of the study and were obtained from Zimbabwe meteorological Office, Harare. Weekly visits were made to the abattoir between October 1985 and September 1986. On each visit 4-9 abomasa of sheep were collected. The origin, sex and age was recorded for each animal. Of 304 animals examined, 212 were 612 months, 44 1-2 years, 20 2-3 years and 20 > 3 years old. The abomasum was slit open in the laboratory. The contents were emptied into a bucket and the mucosa was then washed with water into another bucket. The mucosa was scraped off and digested in H C l - p e p s i n solution overnight at 37 ° C. Either all or half of the samples of contents, washings and mucosal digesta were searched for helminths. RESULTS
Of the abomasa examined, 213 (70%) were found to be infected with H. contortus. The prevalence of infection varied from a minimum of 50% in
M a y to a maximum of 89% in March. The mean monthly worm burden and corresponding meteorological data are presented in Fig. 1. The number of worms increased from December to reach a peak during Febm a r y - M a r c h . This was followed by a sharp decline in April and the numbers remained at a relatively low level until September with certain fluctuations. In general, the number of worms was low between April and November. The proportion of fourth stage larvae (L4) was between 1 and 7% during all the months of the year, except in July and August when 22 and 54%, respectively, of worms were in the L4 stage.
H. CONTORTUS WITH LOW INHIBITEDDEVELOPMENT
349
600m 500. i4OO.
~
300
: 200:~ 1OO0
,
ON
i
i
0
J
i
i
i
,
,
i
,
F MAM
JJuAS
, , . F M AM
~ ~ ; JJuAS
i
200
, . . . . ON D J
~'
(.I o
4
20
-
-
~
-
: ~ . . ~ m a x .
_
:.. ,o 1.... ~
o, O N D J
FMAMJ
JuA$
Fig. 1. Mean monthly maximum and minimum temperature, rainfall and H. c o n t o r t u s burden of sheep.
DISCUSSION The overall prevalence of infection was lower than that recorded by Grant (1981). The worm counts showed a trend which was correlated to the rainfall (Fig. 1). The ideal conditions of rain and temperature would have favoured the development, translation and survival of infective larvae of H. contortus leading to a gradual increase in worm burden from December onwards. The peak burden recorded in February-March can be accounted for by these favourable environmental conditions. The rainfall diminished from March and there was no rainfall from May to September (Fig. 1 ). As the dry cool weather is not conducive to the development of free-living stages (Gordon, 1950 ), there is very little possibility of the acquisition of new infections during this period. This is reflected in a lower worm burden during this period. The proportion of L4 was low throughout the year. Similar results have been found in Kenya (Allonby and Urquhart, 1975), Nigerian savanna and Malaysia (Chiejina et al., 1988). It is possible that our technique for the recovery of
350
v.s. PANDEY
hypobiotic larvae was not sensitive enough and therefore their numbers are underestimated. The recovery of hypobiotic larvae of Ostertagia ostertagi from cattle by the incubation of abomasal mucosa in buffered saline for 24 h is three times higher than the HCl-pepsin digestion used in the present work (Gasbarre, 1987). In a study in Zimbabwe, Grant (1981) recorded 0-10% ofH. contortus as L4 from October to April and 38-72% from May to September. The results in the present study are different. The possible explanation for these differences may be either differences in management or in the weather conditions. The work of Grant (1981) was carried out on a research station where animals received no anthelmintics during the whole period of study. The animals in the present work came from commercial farms where anthelmintic administration is frequent, generally every 2-3 weeks during the rainy season and every 3-5 weeks during the dry season. This difference in anthelmintic treatment is manifested in a lower worm burden in the present work. The annual rainfall during the present period of study was 1036 mm compared with an average of 850 mm in normal years. During the period of study by Grant (1981), the annual rainfall was only 474 mm, a drought situation. It may be that frequent anthelmintic treatment does not allow inhibition of larvae of H. contortus. Alternatively, the very dry conditions during the period of study by Grant (1981), coupled with no anthelmintic medication, were conducive to the inhibition of larvae. Supporting evidence for low inhibition of strongyles comes from an epidemiological study of parasites of donkey from the highveld of Zimbabwe. Very few inhibited larvae of small strongyles were observed even during the dry period of the year (Eysker and Pandey, 1987, 1989). It appears that in the highveld of Zimbabwe, inhibition of strongyle larvae is not important. More controlled work needs to be done to clarify the importance of inhibited larvae in the epidemiology of H. contortus under management conditions of sheep in the highveld of Zimbabwe. This study demonstrates that infection with H. contortus is high during the warm rainy season despite intensive anthelmintic treatment. This seems to be due to the fact that animals are set stocked, often at a high stocking rate. If infection levels are to be reduced, the sheep should be moved to cleaner pastures after anthelmintic treatment. ACKNOWLEDGEMENTS Grateful thanks are due to M. Taruvinga and V. Bhariri for their able technical assistance, to J. Harvey, Manager of Mt. Hampden abattoir, for providing the facilities and to Rosemary Mubaiwa for typing the manuscript.
H. C O N T O R T U S WITH LOW I N H I B I T E D DEVELOPMENT
351
REFERENCES Allonby, E.W. and Urquhart, G.M., 1975. The epidemiology and pathogenic significance of haemonchosis in a Merino flock in East Africa. Vet. Parasitol., 1: 129-143. Chiejina, S.N., Fakae, B.B. and Eze, B.O., 1988. Arrested development of gastrointestinal trichostrongylids in goats in Nigeria. Vet. Parasitol., 28: 103-113. Eysker, M. and Pandey, V.S., 1987. Overwintering of non-migrating strongyles in donkeys in the highveld of Zimbabwe. Res. Vet. Sci., 42: 262-263. Eysker, M. and Pandey, V.S., 1989. Small strongyle infections in donkeys from the highveld of Zimbabwe. Vet. Parasitol., 30: 345-349. Gasbarre, L.C., 1987. Recovery of third-stage larvae of Ostertagia ostertagi from the abomasa of experimentally inoculated calves by prolonged saline incubation. Proc. Helminthol. Soc. Wash., 54: 160-161. Gibbs, H.C., 1982. Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Vet. Parasitol., 11: 25-48. Gordon, H.Mcl., 1950. Some aspects of parasitic gastro-enteritis of sheep. Aust. Vet. J., 26: 14-52, 93-98. Grant, J.L., 1981. The epizootiology of nematode parasites of sheep in a high-rainfall area of Zimbabwe. J. S. Afr. Vet. Assoc., 52: 33-37. Jansen, J. and Pandey, V.S., 1989. Observations on gastro-intestinal helminths of goats in Zimbabwe. Zimbabwe Vet. J., 20: 11-13. Vercruysse, J., 1985. The seasonal prevalence of inhibited development of Haemonchus contortus in sheep in Senegal. Vet. Parasitol., 17: 159-163.