Parasite spectrum and seasonal epidemiology of gastrointestinal nematodes of small ruminants in The Gambia

Veterinary Parasitology, 49 ( 1993 ) 2 7 1 - 2 8 3 0 3 0 4 - 4 0 1 7 / 9 3 / $ 0 6 . 0 0 © 1993 - Elsevier Science Publishers B.V. All fights reserved

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Parasite spectrum and seasonal epidemiology of gastrointestinal nematodes of small ruminants in The Gambia

T. Fritsche *'a, J. Kaufmann b, K.

Pfister b

alnternational Trypanotolerance Centre (ITC), P.M.B. 14, Banjul, Gambia bDepartment of Veterinary Parasitology, University of Berne, P.O. Box 2 735, CH-3001 Berne, Switzerland (Accepted 19 November 1992)

Abstract One hundred and four post mortem examinations of randomly selected sheep (52) and goats (52) were carried out weekly from March 1990 to February 1991. Gastrointestinal parasites were identified and counted. A large spectrum of 16 helminth species was found in 101 (97%) infected animals. The nematodes infecting small ruminants were, in order of predominance: Trichostrongylus colubriforrnis (96% of all animals), Oesophagostomum columbianum (82%), Haemonchus contortus (67%), Strongyloides papillosus (55%), Gaigeria pachyscelis (38%), Cooperia spp. (49%) and Trichuris ovis (12%). Fortyfive (43%) necropsies revealed an infection with Moniezia benedenL Avitellina centripunctata or Stilesia globulosa. Infections with Schistosoma bovis and Pararnphistomum spp. were rarely seen. Goats carried significantly lower worm burdens than sheep and were less often infected by tapeworms. Nematode worm burdens followed a similar seasonal pattern in both host species. While Trichostrongylus colubriforrnis was also recovered in high numbers in the mid dry season, other species such as H. contortus, Strongyloides papillosus and Oesophagostomum columbianum reached distinct peaks in the rainy season (July-October). Different survival strategies for the prolonged dry season were observed. Haernonchus contortus outlived the unfavourable climatic conditions as inhibited larvae in the abomasal mucosa, while the other nematode species survived as adults with a reduced fecundity. Egg production per adult worm specimen was found to depend heavily on the season and egg counts in the dry season ( N o v e m b e r - J u n e ) did not correspond to the size of worm burdens. Unexpectedly high worm burdens were recovered from adult and old animals. Investigations of young animals indicated that no reinfection can occur during the dry season. The findings are discussed with regard to their relevance for strategic control of gastrointestinal nematodes in small ruminants. *Corresponding a u t h o r at Hofwiesweg 3, 9050 Appenzell, Switzerland.

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T. Fritsche et aLIVeterinary Parasitology 49 (1993) 271-283

Introduction

While parasitic diseases of cattle in Africa attract a lot of attention (Murray et al., 1979 ), the contribution of small ruminants to h u m a n nutrition should not be forgotten. Shaw and Hoste ( 1987 ) estimated the small ruminant population in The Gambia to be more than 330 000 animals. With an estimated density of small ruminants of 32 km -2, The Gambia ranks second after Nigeria among all central and West African countries. The rearing of small ruminants is wide spread among the different ethnic groups. Sheep and goats are often owned by female members of the family, and compared with cattle, are less highly valued in terms of prestige and the conservation of capital (Rawlings et al., 1989). The owner's relationship to small ruminants is less pronounced and the animals are more willingly slaughtered or sold to provide for daily requirements. Therefore, it is likely that an increase in production by improved health management, including vaccinations and strategic worm control, could have a direct and beneficial impact on the economic exploitation of small ruminant livestock. The main constraints to rearing small ruminants under the West African savannah conditions include malnutrition during a dry season lasting 7 months (Fig. 1 ), helminth infections and the viral disease 'peste des petits ruminants' ( P P R ) . Of these, the latter two factors could be controlled with acceptable expenditure. With regard to helminth infections, scientists at the Senegal Institute of Rainfall and mean temperatures in Bansang raln 300

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Agricultural Research (1988) reported that a biennial anthelmintic treatment resulted in increased weight gains and a lower mortality and also reduced the age of first lambing and the mortality rate of lambs of treated mothers. They concluded that the mortality due to other diseases, such as PPR, was significantly reduced by deworming. To develop strategic preventive treatments, it is necessary to have a fairly precise knowledge of the seasonal epidemiology of helminth infections in the area (Thys and Vercruysse, 1990). Few data are available on the seasonal dynamics of worm populations in sheep and goats in this region (Vercruysse, 1983 ) and much of it is based on faecal egg counts to estimate corresponding worm burdens. In cattle, however, the egg production of nematodes was found to depend heavily on the season (Kaufmann and Pfister, 1990). During the dry season, when conditions are unfavourable for the development of infective larvae, faecal egg production is reduced. Since the estimation of faecal egg counts is misleading, it is therefore more reliable to quantify the worm burden by post mortem examinations, particularly during the dry season. The aim of this investigation was to study the seasonal epidemiology of helminth infections in small ruminants as a step towards control recommendations for livestock owners. Animals and methods

Animals From March 1990 to February 1991, 104 ante mortem and post mortem investigations of 52 goats and 52 sheep were carried out at regular weekly intervals. The animals were selected at random from the local abattoir in Bansang (M.I.D.), The Gambia. All the animals belonged exclusively to the two breeds of small ruminants reared in this region: Djail~nke sheep (West African Dwarf sheep) and the Guinean goat (West Africafi Dwarf goat). Both breeds are considered to be trypanotolerant (Agyemang et al., 1991 ). During the rainy season (July-October), the grazing of sheep find goats is controlled to prevent crop destruction. The individuals in half of the herds are tethered to wooden pegs which may be moved several times during the day and the remainder are herded by children. After the harvest, the animals are released in the morning and left to roam unsupervised (Greenwood et al., 1989). At night, sheep and goats are housed separately within the compound. Goats are more often provided with a roofed enclosure because they are considered to be more susceptible to the adverse conditions of the wet season than sheep.

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Ante mortem examination An ante m o r t e m investigation was performed on every animal on the evening before slaughter. Various parameters, including village of origin, body temperature, age, sex, body condition and infestation with ectoparasites were recorded and blood and rectal faecal samples taken. The dark ground buffy coat m e t h o d (Murray et al., 1983 ) was used for the detection and quantification of trypanosome infections. Rectal faecal samples were investigated using a flotation and a sedimentation method (Boch and Supperer, 1983 ). For worm egg counts (EPG) and Coccidia oocyst counts ( O P G ) , a modified McMaster technique (Gordon and Whitlock, 1939 ) was used. Post mortem examination Gastrointestinal parasites At slaughter, a post m o r t e m analysis included inspection of the lungs, liver, rumen, heart and carcass. Thereafter, each gastrointestinal tract was removed and the abomasum immediately isolated by two ligatures to avoid mixing of the contents. Thereafter, the abomasum was opened along the major curvature and washed. Abomasal contents and washings were then collected in a bucket and passed through a sieve of 2 0 0 / t m mesh in order to clear the suspension and retain the adult nematodes. Sieve contents were resuspended in 3 1 of water, and after proper mixing, a sample of 200 ml was taken. The small intestine and the caecum with the colon ascendens were slit along their length and processed separately in the same manner as the abomasum. The samples were examined, a few millilitres at a time, in a petri dish under a dissecting microscope (magnification X 25 ). For each intestinal compartment, worms were counted and collected in 4% formaldehyde for subsequent identification after treatment with 90% lactic acid. Female nematodes were identified to genus level and males to species level. Determination was confirmed by taxonomists of the International Institute of Parasitology in St. A1bans, UK. In the caecum, all macroscopically detectable nodules were counted. To estimate the numbers of larvae, the mucosa of the abomasum, the duod e n u m and the caecum were scraped off and separately digested at 37 °C for 12 h in a solution of 1% pepsin and 0.5% HC1 (Herlich, 1956 ). In the digested material the larvae were counted as described for the adults above. An artificial digestion was performed on serial samples of ten excised caecal nodules. Other parasites During the collection of the intestines at the local abattoir the organs of approximately 200 animals slaughtered the same morning were analysed using standard meat inspection techniques.

T. Fritsche et al. /Veterinary Parasiwlogy 49 (1993) 271-283

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In ten additional animals (five goats and five sheep) showing nasal discharge, sneezing or a suspicious ataxia, the crania and the nasal passages were opened to search for Coenurus cerebralis or Oestrus ovis.

Statistical analysis All data were recorded in a database of the Dbase 3.plus program (AshtonTate, 1984) and statistical analysis was performed using the SPSS program. Differences between groups were tested using the Wilcoxon rank-sum test or F-test: P < 0.05 was considered significant. Results

Parasite spectrum Of the 104 animals investigated, 101 (97%) were infected with gastrointestinal nematodes. The three worm-free animals were less than 6 months of age and were born during the dry season of 1989/1990. The prevalence and average numbers of 21 species, belonging to 18 genera of endoparasites and ectoparasites are listed in Table 1. The most c o m m o n nematode species were Trichostrongylus colubriformis, Haemonchus contortus and Oesophagostomum columbianum. Their prevalence in sheep and goats was similar, ranging from 67 to 98%. Strongyloides papillosus and Gaigeria pachyscelis were found often but mostly in moderate numbers. Sheep were more frequently infected with Cooperia spp. and tapeworms, whereas Trichuris ovis was more often recovered from goats (Table 1). The prevalence of Trypanosoma spp. (Trypanosoma vivax and Trypanosoma congolense) parasitaemia was 6% and 15% in goats and sheep, respectively. Two of the three young, worm-free animals acquired Coccidia infections during the dry season and showed very high rates of oocyst excretion. Ticks were only found on sheep. Infection with tick-transmitted parasites (Babesia spp., Anaplasma spp.) was not found in Giemsa-stained blood smears. In none of the inspected animals were infections with Fasciola spp., Dicrocoelium spp., Ecchinococcus spp., Coenurus cerebralis, Oestrus ovis or lung worms discovered.

Seasonality The seasonal dynamics of worm burdens in sheep and goats followed a similar pattern (Figs. 2 and 3 ). In both species, abomasal and small intestinal

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T. Fritscheet aL/VeterinaryParasitology49 (1993)271-283

TABLE 1 Spectrum, prevalence and average burdens of parasites found in small ruminants in The Gambia in 104 post mortem examinations between March 1990 and February 1991 Parasite

Goats Prev.1

Sheep Average

Range 2

(%) Haemonchus contortus Oesophagostomum columbianum Trichostrongylus colubriformis Strongyloides papillosus Gaigeria pachyscelis Cooperia curticei Cooperia punctata Cooperia pectinata Trichuris ovis Moniezia benedeni

67 79 94 60

Other cestodes 4

12 25 6

Cysticercus tenuicollis Paramphistomum spp.5 Schistosoma boris Coccidia spp. Trypanosoma spp. Sarcoptes scabiei Ticks

37 19 2 4 21 6

6 96 6

Prev.

Average

Range

(%) 210 15-1675 81 15- 420 1037 30-5715 442 15-3870 21 2- 105 38 15- 90 165 52 +_+++3 + +-+ + +-++ + + +-+++ 1+ - 6 +

0 0

67 85 98 50 40 65 12 2 4 17 52 17 13 2 94 15 6 35

137 15-1420 24 15- 60 2301 75-7875 211 15-2085 26 1- 180 464 15-3630 175 30- 420 405 +-++ +-+++ +-+ + + + + +-+++ 1+-6+ + +-+ +

1 Prevalence. 2Load range. 3Semi-quantitative estimation.

4Avitellina centripunctata, Stilesia globulosa. 5Calicophoron phillerouxi, Cotylophoron cotylophorum.

burdens increased with the onset of the rains and reached a peak in September/October. A second peak was observed in March/April, after which time worm numbers steadily decreased until the start of the rainy season. Goats carried significantly ( P < 0.001 ) less gastrointestinal nematodes than sheep. This difference was mainly caused by different loads of Trichostrongylus colubriformis, which accounted on average for 76% of the total burdens (sheep 80%, goats 62%). This nematode species was also responsible for the second peak of small intestinal burdens in the mid dry season, when it accounted for 88% of the burdens. Although the parasite inhabits the abomasum and small intestine, 94% of the specimens were found in the latter. Trichostrongylus colubriformis o c c u r r e d as a monoinfection in only 2% of the animals. Haemonchus ontortus burdens reached comparable levels and followed a similar pattern in both host species. Seventy-one percent of adult H. contortus specimens were recovered between August and October (rainy season). Sig-

T. Fritsche et aL/Veterinary Parasitology 49 (1993) 271-283

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nificantly ( P < 0.001 ) higher burdens were found during this 3 m o n t h period. In goats, the mean counts of H. contortus showed a so-called 'rains rise', e.g. the number of adults started to increase 1 m o n t h before the first rain. Counts of abomasal larvae revealed a marked peak in December, thereafter they decreased to a low level for the rest of the dry season. Figures 4 and 5 show that

278

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Fig. 5. Mean abomasal load of goats in the Bansang area. in the early dry season this parasite appeared almost exclusively in the larval stage (94%). Oesophagostomum columbianum burdens showed a large difference between the two host species. While the prevalence o f the infection was high in sheep (85%) and goats (79%), the average burden was much higher in goats

279

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and was clearly concentrated in the wet season. Sheep harboured steady low numbers of oesophagostomes throughout the year and burdens never exceeded 60 specimens per animal (Table 1 ). No correlation was found between the size of burdens and the number of nodular abscesses in the intestinal wall. The average number of these nodules in the large intestine was 112 for sheep and 77 for goats; however, in half of the animals, an uncountable number of nodules was also spread along the small intestine. In 45% of cases, fourth stage larvae (1-.4) could be detected in these nodules by artificial digestion. Strongyloides papillosus occurred mostly in moderate numbers and reached a peak early in the wet season. Gaigeria pachyscelis, Cooperia slap., cestodes, trematodes and Coccidia Slap. occurred throughout the year without seasonal fluctuation. The mean faecal egg output is outlined in Fig. 6. Egg counts remained at a low level during early and mid dry season and increased substantially during the wet season. A similar, but less distinct fluctuation, was observed in the excretion of Coccidia oocysts. The fecundity of the helminths was clearly seasonal. Mean faecal EPG per recovered adult worm (males and females) was 1.17 in September/October and 0.13 in March/April.

Relationship between host age and worm burdens All age groups consisted of 6-20 animals. Young animals born during the dry season did not carry nematodes until after the start of the rainy season.

280

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Fig. 7. Age-burden relationshipof nematode burdens. Animals younger than 1.5 years showed lower burdens than older animals (Fig. 7 ). In sheep, the highest burdens of nematodes (over 2900 ) were found in animals of 1.5-3 years of age, but the total number decreased only slightly in older animals. Sheep older than 4 years still carried an average load of more than 2800 nematodes (range 4 4 0 - 6 8 2 8 ) and their abomasal load was even higher than in younger sheep. In goats, the burdens also decreased after 3 years of age, but increased again in the oldest age group, which harboured a mean load of more than 2000 worms (705-4122 ). In both host species the heaviest H. contortus burdens were found in animals older than 4 years, while Strongyloides papillosus was predominant in younger animals. Discussion This investigation revealed the parasite spectrum and the seasonality of gastrointestinal nematode infections in naturally infected sheep and goats in the West African savannah zone. A nematode infection rate of 97% with an average burden of over 2000 worms indicates that helminthosis forms a highly prevalent infection in Gambian small ruminants. A large spectrum of 16 nematode species was detected (Table 1 ) with Tri-

chostrongylus colubriformis, H. contortus, Oesophagostomum columbianum and S. papillosus being the predominant species. With regard to both prevalence and burden, Trichostrongylus colubriformis was the most common nematode. Unexpectedly, high burdens of Trichostron-

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gylus colubriformis were discovered in the mid dry season (March and April), after which time the worm load decreased steadily until the following rainy season enabled a new generation of infectious larvae to develop. The reduction of Trichostrongylus colubriformis numbers towards the end of the dry season may possibly be the result of a developing immunity which allows the animals to reduce the parasites during a time of low helminth challenge. This can also be due to the expulsion of the old Trichostrongylus colubriformis specimens without reinfection or replacement (self-cure). By contrast, high numbers of H. contortus were discovered exclusively in the wet season (Figs. 4 and 5 ). At the beginning of the dry season high numbers of larvae were found in the abomasal mucosa and the adult Haemonchus burden dropped markedly. No adults were identified in February, and only very few in March and April. This suggests that H. contortus survive the dry season mainly as hypobiotic larvae in the abomasal mucosa, which corresponds to findings in cattle of the same area (Kaufmann and Pfister, 1990). The inhibited larvae possibly represent the source for an early establishment of H. contortus at the beginning of the following rainy season or even before the onset of the rains. Average numbers of Oesophagostomum columbianum, 81 and 24 worms in goats and sheep respectively, with a range not exceeding 450 can be considered as relatively low compared with findings described by Grant ( 1981 ) in Zimbabwe, who found average burdens of 300-470 worms per lamb. The parasite is more c o m m o n in moist climates, because the free-living stages show little resistance to desiccation (Kates, 1950). Nevertheless, the numerous nodular lesions on the intestinal and caecal walls with diameters from 0.2 to 1.5 cm confirm a certain pathological relevance. Furthermore, morphologically undamaged t 4 w e r e located throughout the year from artificially digested nodules. This species is known for its ability to hibernate in a larval stage within these nodules (Dunn, 1978). Nematode egg excretion remained at a low level until the rains had started, in spite of the high numbers of parasites present in March and April. Fecundity, expressed as eggs per gram faeces per adult worm, was nine-fold lower during this period. This is evidence that nematode species surviving the dry season as adults (Trichostrongylus colubriformis, Cooperia spp., Strongyloides papillosus, G. pachyscelis) stay in a hypometabolic state during these months (Kaufmann and Pfister, 1990). Attempts to quantify worm burdens by faecal counts during this period would inevitably lead to a considerable underestimation. Regarding the age/burden relationship (Fig. 7 ), the worm counts for adult animals were unexpectedly high. Animals older than 4 years even carried more H. contortus specimens than animals of all younger age groups. A lack of challenge during the prolonged dry season combined with insufficient nutrition could be responsible for a lack of protective immunity at the start of the fol-

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lowing rainy season (Kaufmann and Pfister, 1990). This age group, therefore, may constitute a major source of pasture contamination. Although clinical helminthosis occurs more often in kids and lambs, old animals should also be included in future control regimes. Worm counts of the youngest age group (less than 1.5 years) may not represent the susceptibility of these animals because the sample includes a considerable proportion of animals weaned at the end, or even after, the rains when no third stage larvae were present. Suckling kids/lambs are less exposed to a contaminated pasture and the season of weaning appears to be of major epidemiological importance with regard to helminth infections. The present observations may initially be of help in the development of strategic control measures. Appropriate drugs, intervals and seasons of treatments for an optimised cost/benefit ratio remain to be established under local field conditions. Three facts merit special consideration. ( 1 ) One month after the last rains up to the beginning of the following rainy season, no infective larvae are present on the pasture (Kaufman et al., 1991 ). Dewormed animals seem not to become reinfected during the dry season. Repeated dry season treatments are therefore unlikely to be beneficial. As a further conclusion, control strategies during the dry season can reach all parasites and their larval stages within the host. Strict control campaigns on all ruminants of a certain area could considerably lower or even avoid a larval pasture contamination of the following rainy season. (2) Haemonchus contortus and Oesophagostornum columbianum can survive the dry season in the larval stage. An overwhelming portion of the H. contortus burden appears as inhibited larvae during that time. Therefore, if dry season treatment is required, a larvicidal drug should be used. (3) Unlike in temperate climates, adult and older animals still carry considerable worm burdens and therefore may suffer from disease and contribute markedly to pasture contamination. Control campaigns should, therefore, also include this age group.

Acknowledgements This study was supported by a research grant of the Swiss Development Cooperation, Switzerland, and initiated by the Department of Veterinary Parasitology, University of Berne, Switzerland. Thanks are expressed to the International Trypanotolerance Centre and the University of Berne Helminthiasis Project, The Gambia, for providing the necessary facilities. The authors wish to express their gratitude to Andrea Inauen for her support in the extensive laboratory work and to Professor G.M. Urquhart for his helpful criticism of the manuscript. The assistance of Dr. J. Zinsstag and Gaby Zuercher is very much appreciated. Thanks are expressed to Dr. Linda M.

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Gibbons and Dr. Arlene Jones, International Institute of Parasitology, St. A1bans UK, for confirming identifications of helminths. References Agyemang, K., Rawlings, P., Clifford, D., Bojang, N. and Tamba, A., 1991. Productivity and health parameters of small ruminants in villages of The Gambia. Bull. Anim. Health Prod., 39: 129-135. Ashton-Tate, 1984. DBase III. Users Manual. Ashton-Tate, Culver City, CA, 546 pp. Boch, J. and Supperer, R., 1983. Veterin~irmedizinische Parasitologie. 3. Auflage. Paul Parey, Berlin and Hamburg. Dunn, A.M., 1978. Veterinary Helminthology, 2nd edn. Heinemann Medical Books, London. Gordon, H. McL. and Whitlock, H.V., 1939. A new technique for counting nematode eggs in sheep faeces. J. Counc. Sci. Ind. Res. Aust., 12: 50-52. Grant, J.L., 1981. The epizootiology of nematode parasites in a high-rainfall area of Zimbabwe. J. S. Afr. Vet. Assoc., 52( 1): 33~37. Greenwood, E., Alloway, E.C., Ehrlich, P.C., Mullineaux, E. and Boddy, J.M., 1989. Royal (Dick) School of Veterinary Studies Research Project in The Gambia 1988/89, pp. 17-18. Herlich, H., 1956. A digestion method for post mortem recovery of nematodes from ruminants. Proc. Helminthol. Soc. Wash., 23: 102-103. Institut S6n6galais de Recherches Agricoles, 1988. L'616vagetraditionnel des petits ruminants dans la zone de Kolda. Document de travail No. 1/Kolda, ISRA, pp. 139-163. Kates, K.C., 1950. Survival on pasture of free-living stages of some common gastro-intestinal nematodes of sheep. Proc. Helminthol. Soc. Wash., 17: 39-58. Kaufmann, J. and Pfister, K., 1990. The seasonal epidemiology of gastrointestinal nematodes in N'Dama cattle in The Gambia. Vet. Parasitol., 37: 45-54. Kaufmann, J., Komma, A. and Pfister, K., 1991. The effect of management on the contamination of night holding areas and infections with gastrointestinal nematodes of N'Dama cattle in the Gambia. Trop. Anim. Health Prod., in press. Murray, M., Mclntyre, W.S.M., Murray, P.K., Urquhart, G.M., Jennings, F.W., Greig, W.A., Clifford, D.J., N'Dowe, W.S.M., Touray, B., Sanyang, B.T. and Bray, R.S., 1979. Cattle diseases and trypanosomiasis in The Gambia. I. Clinical studies. II. Pathology studies. In: 15th Meeting of the Int. Scientific Council for Trypanosomiasis Research and Control, Banjul, The Gambia (unpublished). Murray, M., Trail, J.C.M., Turner, D.A. and Wissocq, Y., 1983. Livestock Productivity and Trypanotolerance. Network Training Manual. International Livestock Centre for Africa, Addis Ababa, Ethiopia (unpublished). Rawlings, P., Agyemang, K., Clifford, D., Bojang, N. and Tamba, A., 1989. Patterns of ownership and management of small ruminants and equines in four localities in The Gambia. Afr. Livest. Res., in press. Shaw, A.P.M. and Hoste, C.H., 1987. Trypanotolerant cattle and livestock development in West and Central Africa. Vol. I. Anim. Prod. Health Pap., 67/1, FAO, Rome, pp. 22-23. Thys, E. and Vercruysse, J., 1990. Est-il encore opportun de pr6coniser la vermifugation syst6matique des petits ruminants d'Afrique sah61o-soudanienne contre les n6matodes gastrointestinaux? Rev. E16v. M6d. V6t. Pays Trop., 43 (2): 187-191. Vercruysse, J., 1983. A survey of seasonal changes in nematode faecal egg count levels of sheep and goats in Senegal. Vet. Parasitol., 13: 239-244.