Effect of subclinical coccidiosis in kids on subsequent trichostrongylid infection after weaning

Veterinary Parasitology, 45 (1993) 177-183 Elsevier Science Publishers B.V., Amsterdam

177

Effect of subclinical coccidiosis in kids on subsequent trichostrongylid infection after weaning C. de la Fuente, M. Cuquerella, L. Carrera and J.M. Alunda Departamento Patologia Animal L Facultad de Veterinaria, Universidad Complutense, 28040 Madrid, Spain (Accepted 25 August 1992)

ABSTRACT De la Fuente, C., Cuquerella, M., Carrera, L. and Alunda, J.M., 1993. Effect of subclinical coccidiosis in kids on subsequent trichostrongylid infection after weaning. Vet. Parasitol., 45: 177-183. Seven-week-oldfemale kids of the Murciana-Granadinabreed naturally infected with coccidia were superinfected with a multispecific Eimeria inoculum ( 300 000 oocysts) or treated to control the coccidial infection with Amprolium (50 mg kg-~ liveweight day-l; 4 days every 14 days ); 80 days later both animal groups received 2500 third-stage larvae of a sheep-derived mixture of Trichostrongylus colubriformis (50%), Teladorsagia circumcincta (40%) and Haemonchus contortus (10%). Kids experimentally superinfected with Eimeria showed reduced food intake at the early patency period, higher numbers of oocysts passed at weaning time and lower liveweight gain than the Amprolium-medicated kids. In the Eimeria superinfected kids the trichostrongyle infection caused a tendency to result in chronic coccidial infections. Further, these animals bad higher numbers of nematode eggs in their faeces, lower dressed weights on slaughter and inferior meat quality.

INTRODUCTION

Goat farming under extensive grazing systems is common in many mediterranean-type climates. Under these operational conditions the majority of the restocking animals, once weaned and put out to graze, are exposed to concurrent or sequential coccidial (Eimeria) and gastrointestinal helminth infections. For this reason, such mixed infections are extremely frequent in all places where significant numbers of goats are bred (Cabaret, 1976; Tarazona Vilas, 1984; Kanyari, 1988a). Nevertheless, to the best of our knowledge, the only information concerning the effect of concurrent Eimeria (Eimeria christenseni) and gastrointestinal nematodes ( Trichostrongylus colubriformis) inCorrespondence to: Dr. J.M. Alunda, Departamento Patologia Animal I, Fac. Veterinaria, 28040 Madrid, Spain.

© 1993 Elsevier Science Publishers B.V. All rights reserved 0304-4017/93/$06.00

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fections in this species, under experimental conditions, has been obtained in 8-month-old pigmy goats (Frandsen, 1982). Bearing in mind the extent of these mixed infections in goats, the important role of coccidiosis in pathology in kids (Yvor6 et al., 1980, 1985; Aumont et al., 1984; Foreyt et al., 1986 ) and of gastrointestinal nematode infections in older animals (Blood and Radostits, 1989), together with both the growing interest in this species (Russel, 1990) due to the high quality of goat products and the scarcity of information available on these animals, we have studied the effect of uncontrolled Eimeria superinfections on subsequent trichostrongylid challenge in weaned female kids. The present paper shows the results of a pilot trial including some clinical (food intake, degree of faecal softening), parasitological and zootechnical parameters, in vivo (liveweight gain, food conversion efficiency) and postmortem (carcass yield and meat quality) results. MATERIAL AND METHODS

Parasites Eimeria oocysts were obtained from a naturally infected goat herd and allowed to sporulate at room temperature in 2.5% potassium dichromate solution under aeration. Sporulated oocysts were washed before experimental infections. The Eimeria inoculum contained 37% Eimeria arloingi, 14% Eimeria alijevi, 12% Eimeria ninakohlyakimovae, 10% Eimeria apsheronica, E. christenseni and Eimeria hirci and lower percentages ofEimeria pallida (6%) and Eimeria jolchijevi (1%) sporulated oocysts. Third-stage larvae (L3) of trichostrongylids (50% Trichostrongylus colubriformis, 40% Teladorsagia circumcincta and 10% Haemonchus contortus ) for the experimental infections were prepared by mixing the appropriate amounts of the monospecific infections maintained in lambs at our department and obtained originally from Merck Sharp & Dohme (Spain). These percentages were selected because of the average findings observed in natural infections in goats in central Spain (Tarazona-Vilas, 1984 ). Kids, experimental design and analyses Eleven female kid goats, approximately 25 days old, of the MurcianaGranadina breed were obtained from a local supplier and were shown to be carrying natural Eimeria infections. Until they were 14 weeks old the kids were fed with a milk replacer; subsequently, the amount of milk was progressively reduced and the animals were fed with pelleted food, lucerne hay and tap water ad libitum. At 7 weeks of age, the kids were distributed into two groups. Group A (five animals) was superinfected at 7 weeks of age with

COCCIDIOSISIN KIDS AND TRICHOSTRONGYLID INFECTION

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300 000 oocysts of Eimeria inoculum, by means of a bucogastric catheter (60 000 oocysts day- 1, 5 consecutive days). Group B (six animals) received a preventive treatment of Amprolium (50 mg kg- 1 liveweight day- 1 ) on a discontinuous basis (4 days treatment, 10 days rest) during the experimental period to control the original coccidial infection. One of the animals from Group A was withdrawn from the experiment on Day 80 (Day 0 was designated the first day of experimental superinfection with Eimeria oocysts ) because of its poor adaptation to solid food. On this day, all kids (four in Group A and six in Group B) received 2500 trichostrongylid L3 (500 L 3 per animal day- ~for 5 consecutive days ) per os. When the goats were 5 ½months old the experiment was stopped and the animals were slaughtered. The clinical condition of the animals was observed daily. Food ingestion was recorded daily during lactation (Group A, Day 47; Group B, Day 46 ); the food conversion efficiency was calculated for some selected periods and faecal softening (faecal wet weight divided by faecal dry weight) was recorded twice a week during the experimental period. After slaughter the carcass weight was determined; meat quality was estimated by studying the dry matter content and the percentage of protein from the dissected masseter muscles. The output ofEimeria oocysts (oocysts per gram of faeces, OPG) was estimated for each kid twice a week during the experiment. Helminth egg counts (eggs per gram of faeces, EPG) were done from Day 80 onwards (Group A) or from Day 82 onwards using the same faecal samples. Output of parasites was determined by a modified McMaster technique (Ministry of Agriculture, Fisheries and Food, 1971 ). In all parameters studied, arithmetic means and standard deviations were calculated. Statistical significance was estimated using Student's t-test. RESULTS AND DISCUSSION

Under our conditions the only clinical signs seen were the episodes of faecal softening observed during the milk replacer feeding period in both groups and inappetence at the time of early patency of the experimental Eimeria superinfection not controlled with Amprolium (Group A). The results obtained by Yvor6 et al. (1985) with multispecific Eimeria infections (E. ninakohlyakimovae, E. arloingi and E. christenseni ) (diarrhoea, weight loss and some deaths) in 8-week-old weaned kids are probably related to the high infective doses employed (200 000 sporulated oocysts from each species). The high pathogenic effect of monospecific E. arloingi infections in 6-week-old kids ( 10 000 oocysts) reported by Sayin et al. (1980) contrasts sharply with our results and could be a consequence of different host sensitivity (Kanyari, 1988b). Moreover, our kids began with a natural infection of coccidia, pos-

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sibly acquired immediately after birth (Yvor6 et al., 1981 ), thus conferring some degree of protection against the experimental Eimeria superinfection. The present results show that preventive treatment with Amprolium (50 mg kg-1 d a y - l ) using our medication schedule did not result in the reductions in OPG reported by Fitzsimmons (1967) or Horak et al. (1969), although Amprolium-medicated kids showed a sustained tendency towards lower OPG counts during the experimental period. The very high OPG values observed in the superinfected goats immediately after weaning (Days 66 and 69, P < 0.05 ) seem to provide evidence of the critical importance of coccidiosis at weaning time (Gregory and Norton, 1986; Foreyt, 1990). Higher OPG counts did not coincide with constipation, as stated by Aumont et al. (1984) and we could not see any positive correlation between faecal oocyst output and the degree of faecal softening (not shown). This agrees with similar findings in lamb coccidiosis (Gregory and Catchpole, 1987 ). After the experimental challenge with trichostrongylids, a tendency towards chronic Eimeria infections was observed in kids superinfected with coccidia, which could be a result of the inability of these kids to control the spread of coccidiosis effectively during the concurrent helminth infection. This is also suggested by the clear leukopenia, probably related to lymphopenia, TABLE 1

Number of eggs per gram of faeces passed by the Eimeria-superinfected (Group A) and the Amprolium-treated kids (Group B) after challenge with 2500 trichostrongylid infective larvae

(a) GroupA kids Kid no.

1 2 3 4

Days posttrichostrongylidchallenge 17

21

24

31

35

37

0 200 100 200

350 1350 1000 50

350 1200 1600 450

1550 550 2600 900

1800 400 2250 2025

750 350 500 750

(b) GroupB kids Kid no.

1 2 3 4 5 6

Days posttrichostrongylid challenge 17

22

24

31

34

36

0 0 75 0 0 0

50 100 50 100 350 50

150 150 100 200 200 150

250 250 150 300 350 150

100 200 150 350 250 250

200 550 550 350 650 150

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181

found in these animals (de la Fuente and Alunda, 1991 ). The lower immune status of the Eimeria superinfected animals could explain the slight shortening of the period to patency of the gastrointestinal helminth challenge and the higher counts of helminth eggs (EPG) (Table 1 ) with some significant differences (Days 17, 24 and 31 post helminth challenge; P < 0.025 ). The effect of coccidiosis upon weight gain and food conversion ratios in infected goats has been notably inconsistent, ranging from pronounced differences (e.g. Aumont et al., 1984 ) to undetectable ones. It is even more difficult to ascertain the effect of subclinical infections. Our results showed that uncontrolled Eimeria infections caused a lower weight gain (Fig. 1 ) and higher food conversion ratio (not shown). The lower weight gain was especially notable at weaning (Days 54 and 68 ), coincident with rises in OPG counts, and emphasizes the critical role played by coccidiosis when small ruminants are stressed (Foreyt, 1990). Such differences were not reduced by the end of the experiment. Table 2 shows the results of the carcass evaluation. In all cases the Eimeria superinfected kids displayed lower values than the medicated animals. This was especially clear when the dry matter content of the dressed carcasses was considered and there were also notable differences between the protein content of the carcasses of the two groups, although these were not statistically significant. Clearly more experimentation is needed but, under our conditions, multispecific Eimeria superinfections of 7-week-old kids subsequently

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Fig. 1. Liveweight gain during the experimental period in E i m e r i a - s u p e r i n f e c t e d ( - - ) and Amprolium-treated (---) kids. Day 0, first day of experimental super-infection with E i m e r i a oocysts. Arrow (~), days of experimental trichostrongylid challenge (2500 [,3). Bars on the upper side of the graph indicate days of Amprolium treatment. *P< 0.005.

182

C. DE LAFUENTEETAL.

TABLE 2 Carcass efficiency and meat quality of Amprolium-medicated (Group B ) and Eimeria-superinfected (Group A) kids after challenge with trichostrongylids Group

Carcass efficiency (% of liveweight )

Dry matter content (g kg-')

Protein content (% of dry matter)

Amprolium-medicated (n=6)

48.78 46.45 51.69 44.12 50.00 50.00 48.51 ± 2.76

264.87 249.52 252.84 259.65 268.02 270.22 260.85 ± 8.36*

75.12 88.00 80.80 79.20 80.84 72.42 79.40± 5,39

46.09 46.83 45.45 46.67 46.26±0.63

246.61 232.59 237.66 243.37 240.06±6.20'

70.00 72.00 75.60 76.80 73.60± 3.15

Mean±SD Non-medicated (n=4)

MeaniSD *P<0.005.

exposed to a gastrointestinal nematode challenge, apparently caused a lower liveweight gain, lower carcass yield and inferior meat quality at slaughter. In addition, superinfected kids had chronic Eimeria infections and higher counts of trichostrongylids, thus suggesting a lower immune status. ACKNOWLEDGEMENTS

The authors wish to thank F. Fontanilla DVM for help with animal care. Funding and animal facilities provided by the Departamento de Patologia Animal I (San±dad Animal), Facultad de Veterinaria de Madrid, are gratefully acknowledged. REFERENCES Aumont, G., Yvor6, P. and Esnault, A., 1984. Experimental coccidiosis in goats. 1. Experimental model. Effects of parasitism on the feeding behaviour and the growth of animals; intestinal lesions. Ann. Rech. V6t., 15: 467-473. Blood, D.C. and Radostits, O.M., 1989. Veterinary Medicine. Baillibre Tindall, London, 1502 PP. Cabaret, J., 1976. Note sur le parasitisme dfi aux n6matodes et aux coccidies chez les espbces domestiques dans la r6gion de Kaedi (Mauritanie). Rev. Elev. M6d. V6t. Pays Trop., 29: 221-226. De la Fuente, C. and Alunda, J.M., 1991. Efecto de las coccidiosis y trichostrongilidosis subclinicas y secuenciales sobre algunos par~imetros hem~iticos del cabrito. Med. Vet., 8: 550-555. Fitzsimmons, W.M., 1967. Amprolium as a coccidiostat for goats. Vet. Rec., 80: 24-26.

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Foreyt, W.J., 1990. Coccidiosis and cryptosporidiosis in sheep and goats. Vet. Clinics N. Am.: Food Anim. Pract., 6: 655-670. Foreyt, W.J., Hancock, D. and Wescott, R.B., 1986. Prevention and control of coccidiosis in goats with decoquinate. Am. J. Vet. Res., 47: 333-335. Frandsen, J.C., 1982. Effects of concurrent subclinical infections by coccidia (Eimeria christenseni) and intestinal nematodes ( Trichostrongylus colubriformis) on apparent nutrient digestibilities and balances, serum copper and zinc, and bone mineralization in the pigmy goat. Am. J. Vet. Res., 43: 1951-1953. Gregory, M.W. and Catchpole, J., 1987. Output of coccidial oocysts (particularly Eimeria crandallis) by naturally-infected lambs: daily and hourly patterns and clinical significance. Dtsch. Tieriirztl. Wochenschr., 94: 521-525. Gregory, M.W. and Norton, C.C., 1986. Caprine coccidiosis. Goat Vet. Soc. J., 7: 32-34. Horak, I.G., Raymond, S.M. and Louw, J.P., 1969. The use of Amprolium* in the treatment of coccidiosis in domestic ruminants. J. S. Afr. Vet. Med. Assoc., 40: 293-299. Kanyari, P.W.N., 1988a. Coccidiosis in goats and aspects of epidemiology. Aust. Vet. J., 65: 257-258. Kanyari, P.W.N., 1988b. Experimental infections with coccidiosis and serum antibody quantiration in two breeds of goats. Vet. Parasitol., 28:11-18. Ministry of Agriculture, Fisheries and Food, 1971. Manual of Veterinary Parasitological Laboratory Techniques. Her Majesty's Stationery Office, London, 131 pp. Russel, A., 1990. Goats for milk production. In Practice, 12: 179-182. Sayin, F., Dinner, S. and Milli, O., 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. Veterinaermed. Reihe B, 27: 382-397. Tarazona-Vilas, J.M., 1984. Parasitic gastroenteritis in goats in Spain. In: Les Colloques de I'INRA, No. 28. Les Maladies de la Ch6vre. INRA, Paris, pp. 507-512. Yvor6, P., Dupr6, P., Esnault, A. and Besnard, J., 1980. Experimental coccidiosis in the young goat: parasitic development and lesions. Int. Goat Sheep Res., 1:163-167. Yvor6, P., Esnault, A. and Guillimin, P., 1981. La coccidiose du chevreau en 61evage en ch6vrerie: importance du choix du moment du traitement. Rev. M6d. V6t., 132: 205-208. Yvor6, P., Esnault, A. and Naciri, M., 1985. La coccidiose caprine effect de contaminations mono ou multisp6cifiques. Rec. M6d. V6t., 161:347-351.