EXPERIMENTAL COCCIDIOSIS IN GOATS. 2. EFFECT OF PARASITISM ON NUTRITIONAL BALANCES AND SOME BLOOD PARAMETERS

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1 EXPERIMENTAL COCCIDIOSIS IN GOATS. 2. EFFECT OF PARASITISM ON NUTRITIONAL BALANCES AND SOME BLOOD PARAMETERS G. Aumont, P. Yvore, A. Esnault To cite this version: G. Aumont, P. Yvore, A. Esnault. EXPERIMENTAL COCCIDIOSIS IN GOATS. 2. EFFECT OF PARASITISM ON NUTRITIONAL BALANCES AND SOME BLOOD PARAMETERS. Annales de Recherches Vétérinaires, INRA Editions, 1986, 17 (2), pp <hal > HAL Id: hal Submitted on 1 Jan 1986 HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

2 EXPERIMENTAL COCCIDIOSIS IN GOATS. 2. EFFECT OF PARASITISM ON NUTRITIONAL BALANCES AND SOME BLOOD PARAMETERS G. AUMONT P. YVORE A. 2ESNAULT 1 : lnra, CR de Theix, Laboratoire des Maladies Nutritionnelles, Ceyrat France 2: lnra, CR de Tours-Nouzilly, Station de Pathologie Aviaire et de Parasitologie, Monnaie, France Résumé COCCIDIOSE EXPÉRIMENTALE CHEZ LA CHÈVRE. 2. EFFET DU PARASITISME SUR LES COMPO- SANTES NUTRITIONNELLES ET CERTAINS PARAMÈTRES SANGUINS. &horbar; L infection expérimentale de caprins par trois espèces de coccidies, Eimeria ninakohlyakimovae, E. arloingi et E. christenseni, en l absence de signes cliniques apparents, entraîne des modifications importantes des digestibilités apparentes et des balances nutritionnelles de la matière organique, de la matière sèche et de la cellulose. La phase aigue de l excrétion oocystale est caractérisée par une balance azotée négative et une chute l albuminémie, de la glycémie et de l hématocrite. Ces modifications ne peuvent être que partiellement expliquées par la chute de la matière sèche ingérée et les lésions intestinales observées. Numerous studies have shown that subclinical gastro-intestinal parasitism can cause significant losses in all domestic ruminant species. However very little data exist concerning the physiopathology of these losses. We have reproduced a subclinical coccidiosis in young goats. Parasitological investigations described in the first part of this study (Aumont et al., 1984), showed high level of oocysts in faeces three weeks after inoculation with only mild clinical symptoms. We have studied the effect of this parasitism on nutritional balances and some blood parameters. Materials and Methods Tests were carried out on five young male goats of 8-9 month of age, kept coccidia free until experimental inoculation and placed in metabolism cages for goat (Giger and Hervieu, 1980) according to the conditions described in part 1 (Aumont et a/., After three weeks of adaptation to the regime and the cage the tests were performed over periods of 7 days and the results were based on the mean of 5 daily observations to minimize the effect of short term fluctuations. The digesta rate of passage was constant and equal to 24h. Intake of Dry Matter (DMI), water drunk, faeces and urines were weighed daily to calculate apparent digestibility (ad). For technical reasons, sweating and respiration losses of water and minerals were not taken into account. Data for each goat were collected over seven periods (periods I to VII) : two periods during the 15 days before infection (periods I and II) and five periods from the 8th to the 42nd day after infection (DAI) (periods III to Vil). The animals received 1800 g of Alfafa hay and mineral supplement with added vitamin (MSV). The daily rations were prepared before the start of the experiment ensuring that the composition was always the same. All the animals were infected the same day (Do) by a

3 single inoculum of an aqueous suspension containing 3 x 10 8 sporulated oocysts of essentially three species of coccidia : E. ninakohlyakimovae (31%), E. christenseni (25%) and E. arloingi (44 %). Faeces and uneaten forage and MSV were dried and ground for analysis. Sulphuric acid solution (30%) was added to urine (50 ml/kg). The daily output of urine was weighed, and samples for each period kept at 4 C until analysis. Determinations of organic matter (OM), mineral, total nitrogen (Kjeldahl), crude fibre (C+) (Weende). calcium (atomic absorption spectrophotometry), phosphorus (colorimetry), magnesium (atomic spectrophotometry), sodium and potassium (flame photometry) were made in forage and faecal matter. Total nitrogen (Kjeldahl), phosphorus (Mongin and Sauveur, 1976), calcium (photometry after dry incineration), sodium and potassium (Licois et al., 1978) were determinated in urine. Blood samples were taken two or three times a week and determinations made of packed cell volume (PCV), serum albumin, urea, glycaemia (Boehringer Kit) serum sodium and potassium concentrations and blood ph (Licois et al., The non-parametric statistical methods used are described in part 1 (Aumont et al., All differences indicated are significant for 0.01 risk. Results The results of parasitological obervations are described in part 1 (Aumont et al.,

4 Nutritional balances 1.1. Dry matter, organic matter, crude fiber, nitrogen Dry matter intake (DMI) decreased three weeks after infection as was described in part 1 (Aumont et al., 1984). Apparent disgestibility and dry matter were significantly higher (7 to 32 %) during the third week following inoculation (fig. 1 The apparent digestibility of organic matter and crude fibre followed the same kinetics as that for dry matter (fig. 1) despite the variations recorded in composition of DMI (Aumont et al., 1984). Variations in nitrogen intake were similar to those in DMI but there was a large increase nitrogen loss in faeces and urine during periods IV and V (fig. 2). A drop in apparent digestibility of nitrogen was recorded in period V (&horbar; 4.8 % to &horbar; 45.5 %). At the same time, nitrogen balance became negative (fig. 2) and was remained at a low level despite the return to a normal intake Minerals and water We were unable to link any variations in apparent disgestibility of minerals to parasitism. The calcium and phosphorus content of urine remained stable (70 mg/i and 150 mg/i respectively). No variations in calcium and phosphorus balance (0.2 g/d and 6.2 g/d respectively) were noted despite a large decrease in the intake of these minerals during 3rd, 4th ant 5th weeks after inoculation (-17 to 75 96, - 4 to , - 8 to 96, for Ca, P, Mg respectively). Sodium and potassium intake declined from period III and reached a minimum level in period Vi (- 6 to , - 15 to for Na and K respectively). However no significant variation in potassium balance (3.2 g/d) was noted whereas sodium balance fell from 1.7 g/d to 0.5 g/d (fig. 3). The apparent digestibility of sodium and potassium was constant at 90 ant 93 % respectively. Daily water intake of each animals was directly correlated (P < 0.001) with D M 1. The water balance was lowest during the 4th and 6th weeks after infection (fig. 4).

5 - the - the - the 2. Blood parameters Serum albumin concentration decreased from the l3th to the 31 th day after inoculation (fig. 5). Six weeks after inoculation the values remained at a low level. No significant variation was recorded in serum urea concentration but a transient and slight decrease in serum glucose appeared 23th day after inoculation (fig. 6). Packed cell volume decreased from the 13 th day after inoculation to the end of the experiment (fig. 7). Serum sodium and potassium concentration remained constant at mg/i and 5.4mg/i respectively. Blood ph varied between 7.39 to Discussion The experimental infection we produced, caused a very large oocysts excretion but without any obvious clinical signs. However, the dramatic fall in D M I and the change in Dry Matter content of faeces (constipation or momentary diarrhoea) would be associated with considerable variations in digesta flow. Electromyographical studies have shown a reduction and distortion of cyclic intestinal motility in ruminants (Ruckebusch et al., 1975 : Bueno et al., 1980a) and horses (Bueno et a/., 1980b) infected by gastrointestinal helminths. A decrease in D M I and specific actions of worms are involved in these disturbances (Fioramonti and Ruckebusch, 1979). In our study, this alteration in the flow of intestinal digesta was certainly the cause of errors in computing apparent digestibility and nutritional balances. It would be necessary to get more data on relationships between parasitism and some digestive functions (food intake ; rumination rhythms ; total and local passage rate of the healthy and parasitised areas) in order to better adapt methods for such studies. Nevertheless, the fact still remains that in our model, coccidial parasitism caused a significant though transient modification in apparent digestibility of dry matter, organic matter and crude fibre. Barger et al., ( 1973) noted a reduction in apparent digestibility of dry matter in 8 month-old ewes infected by T. colubriformis. Whereas Shumard et al. (1957) recorded an increase in apparent digestibility of crude fibre in sheep infected with abomasal and intestinal helminths. At least three causes may be involved in the increase we observed in apparent digestibility of dry matter during the third week of parasitism evolution : concomitant drop of dry matter ingestion, which is the first disruption caused by parasitism ; disturbances in the flow of digesta. Despite the lack of clinical signs, rate of passage was certainly reduced by parasitism and the fall in D M I. This decline might have led to an increase in ruminal and caecal fermentation and hence a rise the apparent digestibilities of dry matter, organic matter and crude fibre ; changes in quality of D M I being more digestible as a result of marked selection activity (Aumont et al., The drop in the apparent digestibility of nitrogen during the 4th week following infection is a very common phenomenon in infections confined to the intestine (Sykes and Coop, 1976 ; Sykes et al., 1979). It may be explained by the flat mucosa (atrophy of villi) and the probable decrease in enzyme activity which has already been observed in coccidiosis of calf (Benz and Ernst, and rat (Duszynski et al., On the other hand, endogenous nitrogen might have increased by the escape of proteins in intestinal tract due to a rise

6 of intestinal mucosa permeability (Cobden et al., 1979) and erythrocyte turnover ratio. The first cause of the drop of nitrogen balance seems to be the fall in D M I, losses via urine being only slight and uremia remaining unchanged. Hypoalbuminaemia is traditionally found in intestinal parasitism. This reduction in extracellular protein nitrogen may be due to hypercatabolism and a greater turn over rate of these proteins (Mulligna, 1972). Reduction of nitrogen intake and leakage of plasma protein into tissues are certainly involved in this phenomenon. Much more complex techniques must be carried out to understand the nitrogen metabolism caused by subclinical intestinal parasitism. This has been initiated by Roseby and Long ( 1974) and Roseby (1977a). It is difficult to explain the transient and slight hypoglycaemia observed. Hyperglycaemia (Shumard, 1957 ; Shumard et al., 1957) and hypoglycaemia (Mapes and Coop, 1973 ; Roseby, 1977a, 1977b) have both been recorded during intestinal parasitism of lambs. However the large fall in energy balance could cause hypoglycaemia. Whith regard to the major mineral elements, no effects of parasitism development were recorded except for that on sodium balance. However, Barger et al. (1973) and Sykes and Coop (1976) have noted a decrease in apparent digestibility of calcium and phosphorus in lambs chronically infected with T. colubriformis. In our experience the intake of calcium, phosphorus, magnesium and potassium never dropped below the required level. Diarrhoea is a classic symptom of infection by coccidia. In our experiment, slight constipation was more often the sign of parasitism. Despite the very extensive lesions observed on post-mortem, neither the blood ph, sodium nor potassium concentration showed significant disturbances as has been noted in bovine coccidiosis (Fitzgerald and Mansfield, 1972). However water intake was significantly reduced and the decrease in urinary output of water was not sufficient to prevent a fall in water balance when the effects of the infection were at their most severe levels. The subclinical coccidial parasitism with high oocyst output and extensive intestinal lesions had produced reduced growth rate and slight anaemia (Aumont et al., 1984). Taking into account the degree of parasite development and the extent of lesions observed at the end of the experiment (Aumont et al., 1984), the effect of parasitism demonstrated were surprisingly mild. The decrease in D M I and water ingestion can explain negative balance of some elements and fall in empty body weight. Feeding behaviour, areas of intact intestine and physiological homeostasis may compensate for the damage caused by intestinal parasitic development. Studies using methods of analysis of kinetic digesta and nutrient flow would lead to a better understanding of non immunologic resistance to large scale parasitism. This might help to explain the differences between clinical and subclinical parasitism which might be economically important. Revised, l9th March 1985 Revised version, 25th October 1985 Accepted, 30th October 1985 Summary Experimental infection of goats with three species of coccidia (E. ninakohlyakimovae, E. arloingi, E. christensem 1 caused a significant modification in apparent digestibility of dry matter, organic matter and crude fibre but only mild clinical effects. Nitrogen balance became negative and there was a decrease in serum albumin and glucose concentration and packed cell volume. These modifications may be partially explained by the fall of dry matter intake, the change in dry matter content of faeces and the disturbances of intestinal functions. References AUMONT G., YVORE P., ESNAULT A., Experimental coccidiosis in goats. 1. Experimental model. Effect of parasitism on the feeding behaviour and the growth of animals ; intestinal lesions. Ann. Rech. Vet., 15, BARGER LA., Trichostrongylosis and wool growth. 1. Feed digestibility and mineral absorption in infected sheep. Aust. J. Exp. Agric. Anim. Husb., 13, BARGER LA., SOUTHCOTT W.H., WILLIAMS V.J Trichostrongylosis and wool growth. 2. The wool growth response of infected sheep to parental and duodenal cysteine and cysteine supplementation. Aust. J. Exp. Agric. Anim. Husb., 13, BENZ G.W., ERNST J.W., Alkaline phosphatase activities in intestinal mucosa from calves infected with Cooperia punctata and Eimeria bovis. Am. J. Vet. Res., 37,

7 BUENO L., FIORAMONTI S., RUCKEBUSCH Y., 1980a. Digestive disturbances in ruminants : an electromyographic study. Vet. Sci. Com., 4, BUENO L., RUCKEBUSCH Y., DORCHIES P., 1980b. Disturbances of digestive motility of horses associated with Strongyle infection. Vet. Parasitol., 5, COBDEN L, ROTWELLJ., AXON A.T.P., Intestinal permeability in rats infected by Nippostrongylus brasiliensis. Gut, 20, DUSZYNSKI D.W., ROYS A., CASTRO G.A., Intestinal disaccharidase and peroxidase deficiencies during Eimeria nieschulzi infections in rats. J. Protozool., 25, FIORAMONTI J., RUCKEBUSCH Y., Diet and caecal motility in sheep. Ann. Rech. Vet., 10, FITZGERALD P.R., MANSFIELD M.E., Effects of bovine coccidiosis on certain blood components, feed consumption and bodyweight changes in calves. Am. J. Vet. Res., 33, GIGER R., HERVIEU J., Conception d une cage bilan adaptée à la chèvre en lactation. Ann.Zoorechn., 29, LICOIS D., COUDERT P., MONGIN P., Changes in hydromineral metabolism in diarrhoeic rabbits. 1. A study of the changes in water metabolism. Ann. Rech. Vet., 9, MAPPES C.J., COOP R.L., The fate of multiple doses of infective larvae of Nematodirus battus in 8 month-old lambs and their effect on intestinal enzyme activity. /nt.j. Parasito/., 3, MONGIN P., SAUVEUR B., Composition minérale des matibres premidres utilisées couramment en alimentation animale. Indust.Aliment.Anim., 9, MULLIGNA W., The effect of helmintic infection on the protein metabolism of the host. Proc. Nutr. Soc., 31, ROSEBY F.B., 1977a. Effects of Trichostrongylus colubriformis (Nematode) on the nutrition and metabolism of sheep. 3. Digesta flow and fermentation. Austr.J.Agric.Res., 28, ROSEBY F.B., 1977b. Effects of Trichostrongylus colubriformis (Nematode) on the nutrition. 4. Glucose metabolism. Austr. J. Agric. Res., 28, ROSEBY F.B., LONG R.A., Effects of Trichostrongylus colubriformis (Nematode) on the nutrition and metabolism of sheep. 2. Metabolism of urea. Aust.J.Agric. Res., 25, RUCKEBUSCH Y., BUENO L., Electrical activity of the ovine jejunum and changes due to disturbances. Am. J. Dig. Dis., 20, SHUMARD R.F., Studies on ovine coccidiosis. 1. Some physiological changes taking place in experimental infections with Eimeria ninakohlyakimovae (Yakimov and Raslegaeva, 1930) and Eimeria faurei (Moussu and Marotel, 1901 ). J. Parasitol., 43, SHUMARD R.F., BOUN D.W., EVELETH D.F., Physiological and nutritional changes in lambs infected with the nematodes : Haemonchus contortus, Trichostrongylus colubriformis and Nematodirus spathiger. Am.J. Vet. Res., 18, SYKES A.R., COOP R.L., Intake and utilization by growing lambs with parasite damage to the abomasum or small intestine. Proc. Nutr. Soc., 35, 13-14A. SYKES A.R., COOP R.L., ANGUS M.W., Chronic infection with Trichostrongylus vitrinus in sheep. Some effects on food utilization, skeletal growth and certain serum constituent. Res. Vet. Sci., 26,