Effect of Eimeria acervulina Infection on Nutrient Retention with Special Reference to Fat Malabsorption in Chickens V. D. Sharma and M. A. Fernando*

ABSTRACT Nutritional balance studies were conducted to determine the effect of Eimeria acervulina infection on the retention of nutrients and the efficiency of utilization of protein and energy in the diet during the course of intestinal coccidiosis in chickens. Both light and electronmicroscopic studies were conducted to elucidate the pathogenesis of fat malabsorption in the infected chickens. The infection with E. acervulina during the acute phase of the disease (day 4 to day 8 postinfection) caused a reduction (P < 0.01 ) in the retention of percent protein, percent ether extract and percent gross energy of the diet with a concomitant increase (P < 0.01) in the concentration of ether extract and gross energy of the excreta. The metabolizable energy value of the diet was also depressed during this phase. During the recovery phase of the disease (day 9 to day 13 postinfection) infected chickens voided excreta containing a slightly greater concentration of ether extract when compared to the controls but differences in the retention of percent protein and percent gross energy were no longer observed. An increased retention of percent phosphorus also occurred during the recovery phase. Studies involving the carcass composition revealed that the efficiency of utilization of protein and metabolizable energy of the diet for tissue deposition was reduced (P < 0.05) during day 0 to day 8 postinfection but only the efficiency of metabolizable energy utilization was found

*Department of Pathology, University of Guelph, Guelph, Ontario. Reprint requests should be addressed to Dr. Fernando. Submitted 'November 5, 1973.

14.6

to be depressed (P < 0.05) when data for day 0 to day 14 postinfection were analyzed. Both light and electronmicroscopic studies of the duodenal villi of infected chickens during day 5 to day 6 postinfection revealed accumulation of large globules of fat in the villus epithelial cells parasitized by the gammonts of E. acervulina indicating a possible blockade of "fat exit" from these cells.

RESUME Cette experience visait it etudier l'equilibre nutritif, afin de determiner l'effet de la coccidiose intestinale aviaire due it Eimeria acervulina sur la retention des principes nutritifs et sur l'efficacite de l'utilisation des proteines et de l'energie de la diete. On utilisa la microscopie ordinaire et electronique pour elucider la pathogen&se de la malabsorption lipidique, chez les oiseaux parasites. Au cours de la phase aigue de cette coccidiose, c'est-a-dire du quatrieme au huitieme jour apres l'infection, il se produisit une diminution (P < 0.01) dans la retention du pourcentage des proteines, des lipides et de l'energie brute de la diete; on observa en meme temps une augmentation (P < 0.01) de la quantite de lipides et d'energie brute dans les dejections. On nota aussi une diminution de la valeur de l'energie metabolisable de la diete. Durant la convalescence, c'estai-dire du neuvieme au 13e jour apres l'infection, les dejections des poulets experimentaux contenaient un peu plus de lipides que celles des oiseaux temoins; on ne decelait cependant plus de difference dans la retention du pourcentage des proteines et de l'energie brute; il se produisit aussi une retention plus elevee de phosphore. Les etudes relatives a la composition des carcasses revelerent que l'efficacite de la re-

Can. J. comp. Med.

tention des proteines et de l'energie metabolisable de la diete, normalement integrees aux tissus, subissait une diminution (P < 0.05), jusqu'au huitieme jour apres l'infection; toutefois, 1'analyse des donnees portant sur les 14 jours ulterieurs a l'infection ne rev4la qu'une diminution de l'efficacit de l'utilisation de l'energie metabolisable. L'examen des villosites duodenales des poulets parasites, du cinquieme au sixi?eme jour apres l'infection, par la microscopie ordinaire et ilectronique, revela l'accumulation de globules de gras volumineux dans les cellules epitheliales parasitees par des gamontes d'Eimeria acervulina, indice d'un blocage probable de la sortie du gras de ces cellules.

croscopic studies of the intestinal epithelial cells was conducted to elucidate the mechanism of fat malabsorption in infected chickens.

MATERIALS AND METHODS

A total of 270 day old male White Leghorn chickens (University of Guelph, Poultry Farm) were allotted at random to 27 groups of ten chickens each. The chickens were raised in electrically heated batteries under continuous lighting with feed and water provided ad libitum. Nine replicates of ten chickens were allotted at random to one of the three dietary levels of 16, 20, 24% crude protein. The experiINTRODUCTION mental diets were essentially of a corn-soybean meal as previously described (25). Coccidiosis in human subjects caused by Prior to infection the chickens were kept the protozoan parasite Isospora belli is for 15 days on each dietary treatment. On characterized by atrophic changes with flat- the 16th day one group of chickens from tening of the villi, excessive infiltration of each dietary treatment was killed by certhe lamina propria with round and plasma vical dislocation and their carcasses frozen. cells and marked distortion of epithelial Four replicates of ten chickens from each cells of the upper jejunum (7). These dietary treatment were artificially infected changes are clinically manifested by diar- with 100,000 sporulated oocysts of E. acerrhoea and steatorrhea (3, 7). Intestinal vulina per chick while the remaining four coccidiosis in chickens caused by Eimeria replicates served as controls. The chickens acervulina is also characterized by changes were weighed as groups on day 0 (day of in the villus pattern to blunt, greatly short- infection) and on day 8 postinfection. One ened mucosal projections accompanied by metabolism trial was conducted between abnormalities in epithelial cell differentia- days 4 and 8 postinfection. Feed consumption (6, 22) and clinically manifested by a tion of chickens during the metabolism reduction in weight gain (37) or in actual trial was determined. The total quantity loss of weight (10). Weight reduction in of excreta voided by chickens of each pen E. acervulina infection has been attributed was collected separately and accumulated to a reduction in feed and water intake for the duration of metabolism trial. The (23), reduction in the rate of absorption accumulated feces were frozen for later of glucose (8, 19, 21), histidine (19, 21), chemical analysis. On the ninth day after Vitamin A (12), zinc and oleic acid (35) infection the chickens were weighed as and to the loss of plasma proteins as a re- groups and two replicates of chickens per sult of increased permeability of intestinal dietary treatment for each infection group mucosa for the passage of plasma protein were killed and their carcasses frozen. The into the intestine (4, 13, 20, 24). Little is remaining chickens were fed on their reknown, however, regarding the changes in spective diets until the 14th day postinfecthe absorption and retention of nutrients as tion when these chickens were also killed affected by the coccidial infection. The oW and their carcasses frozen. A second metajective of the present study was to deter- bolism trial was conducted with these mine the effect of E. acervutina infection chickens between day 9 to day 13 postinfecon the retention of nutrients during the tion. Random samples of each diet were acute and recovery phase of this infection. obtained on each day of the two metabolism Since the level of dietary protein also af- trials for chemical analysis. The total excreta voided per each pen fects the course of E. acervulina infection (25) the nutrient retention was investigated for each metabolism trial were dried by in chickens fed at various levels of dietary lyophilization and the lyophilized samples crude protein. Both light and electronmi- were pulverized and subjected to chemical

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analysis. Both feed and excreta samples were analyzed for nitrogen, ether extract, ash, calcium and phosphorus by standard procedures (2). The gross energy concentration in feed and exereta was determined by igniting the samples in an oxygen bomb calorimeter (Par Oxygen Co.). The metabolizable energy (ME) value of the diet was calculated by methods described (15). The frozen chicken carcasses were ground in a tissue mincer and duplicate random samples of the completely homogenized tissue mass were taken for lyophilization. The lyophilized tissue was ground and mixed in a waring blender, remixed by hand and analyzed for nitrogen (2) and for gross energy concentration by ignition of a sample in an oxygen bomb calorimeter. The percent protein in the carcass was determined as % nitrogen x 6.25. The data of body weight and nitrogen and gross energy concentration of the carcasses were used to determine the retention of protein and energy by the chickens. The efficiency of utilization of protein and ME between day 0 to 8 and day 0 to 14 postinfection was calculated as nutrient retained expressed as fraction of the total intake of protein and metabolizable energy intake respectively by the chickens during the same period. All data on nutrient retention and efficiency of utilization of protein and ME were subjected to analysis of variance according to standard procedures (30). Tissues for light and electronmicroscopic studies were taken from two week old male White Leghorn chickens raised in a coccidia free environment and infected with 500,000 sporulated oocysts of E. acervulina. Two chickens, each from infected and control groups were killed on days 4, 5 and 6 postinfection and tissue samples were obtained from the distal part of the duodenum and the most proximal part of the jejunum, fixed in 3% glutaraldehyde in Millonig buffer (16) at 4°C, processed and stained for light and electronmicroscopy as described previously (5).

RESULTS The results of nutrient retention and the concentration of fat and gross energy in the feces on the infected chickens along with the metabolizable energy (ME) value

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of the diet are summarized in Table I. Infection with E. acervulina in the acute phase reduced (P < 0.01) the percent retention of protein, ether extract (P < 0.01) and ME (P < 0.01). The retention of ash, calcium and phosphorus was not affected by the coccidial infection. Chickens infected with E. acervulina voided exereta containing a greater (P < 0.01) concentration of fat and gross energy. The ME value of the diet was also reduced (P < 0.01). The effect of E. acervulina infection on nutrient retention was similar on all three levels of dietary crude protein. An increase in the level of dietary crude protein caused a linear decrease (P < 0.01) in the retention of protein and a quadratic effect (P < 0.01) on the retention of ether extract. The percent ether extract retention was increased when the level of dietary crude protein increased from 16% to 20% but decreased on further raising the level of dietary protein level to 24%. The retention of phosphorus also indicated a similar pattern. Level of dietary protein also affected the concentration of ether extract in the feces. The fecal ether extract concentration decreased on increasing the dietary crude protein level from 16% to 20% but increased when the level of protein in the diet was increased from 20% to 24%. During the recovery phase of E. acervulina infection, i.e. days 9-13 postinfection (Table II), a small but significant (P < 0.05) difference in the retention of ether extract persisted. The concentration of ether extract and gross energy of the excreta voided by the infected chickens also remained elevated (P < 0.05) but differences in the retention of protein and energy were no longer observed. The ME value of the diet also returned to the control value. An increased retention of phosphorus (P < 0.01) occurred in the infected chickens during the recovery phase. No significant diet x infection interaction was observed in the retention of nutrients, ether extract and gross energy concentration of the excreta or in the ME value of the diet during the recovery phase. The effect of dietary protein on nutrient retention and fecal fat concentration as observed during the acute phase also persisted during the recovery phase. The efficiency of utilization of dietary protein and metabolizable energy for deposition as tissue protein and energy in

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the infected chickens (Table III) was markedly reduced (P < 0.01) during days .4 0 to 8 postinfection. The difference in the efficiency of protein utilization between the control and infected chickens tend to be greater than the difference in the efficiency of energy utilization. Statistical analysis of the pooled data for days 0 to 14 postinfection for protein and ME revealed that only the difference in the efficiency of protein utilization between the infected and control chickens persisted (P < 0.05) but no significant difference in the efficiency of ME utilization was evident. Accumulations of homogenous material, resembling fat globules were seen in a majority of villus epithelial cells of the intestinal villi parasitized by E. acervulina gamonts four and five days postinfection. These were seen at the light microscope level in 1 ,um Epon sections of tissues post fixed in Osmium tetraoxide and stained with Toluidine blue (Fig. 1). The globules were not seen in Hematoxylin and Eosin stained paraffin sections fixed in Serra's fluid. Similar globules were seen in electronmicrographs of parasitized villus epithelial cells four and five days postinfection (Fig. 2). In these it appeared that the globules were membrane bound. Neighbour- Fig. 1. E. acervulina parasitized villus epithelal cells containing fat globules (arrows), 1 Fm Epon section ing non-parasitized areas of the villi were stained with Toludin blue. X360. free of these fat globules. Duodenal epithelial cells containing other stages of parasitic schizonts in the normal areas of in- the recovery phase, i.e. days 9 to 14 postfected gut and the uninfected controls were infection. This coincides with the compenalso devoid of this lipid material. satory growth of E. acervulina infected chickens observed during this phase (25). An increased rate of nitrogen retention in E. acervulina + E. necatrix infected 1.

DISCUSSION The results of the present study indicate that E. acervulina infection has a profound effect on the protein metabolism of the host during the acute phase of intestinal coccidiosis. Both nutrient retention and chemical composition of chicken carcass indicated that protein retention was decreased during the acute phase and approached the rate of protein retention of the controls during days 9 to 14 postinfection. Since the efficiency of utilization of dietary protein for tissue protein synthesis was depressed during days 0 to 8 postinfection but remained unchanged during the entire days O to 14 postinfection suggests a possible greater rate of protein anabolism during

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Fig. 2. E. acervulina gamonts five -days postinfection (p) with accumulated fat globules (f). X4360.

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TABLE III. Effect of Eimeria acervulina Infection on the Efficiency of Utilization of Protein and Metabolizable Energy of the Diet for Tissue Synthesis

Level of Crude Protein in the Diet % 16 20 24

Days Postinfection 8 14 8 14 8 14

Efficiency of Utilization of Dietary Protein for Tissue Protein Synthesis Control 47.31 i 1.71 48.60 : 1.50 40.06 h 2.95 44.95 :+1 4.55 42.65 + 1.83 46.90 + 3.70

chickens during the tenth week postinfection has also been reported (18). Earlier Turk (34) reported that the digestion and absorption of dietary protein was slightly increased during the acute phase and a further increase occurred during the recovery phase of E. acervulina infection in chickens. Although the rate of absorption of methionine, glycine and arginine was also reported not to be affected during the acute phase the rate of methionine absorption was reported to be increased during the recovery phase of this infection (36). On the contrary the absorption of amino acid histidine was found to be depressed during the acute phase of E. awervulina infection (21). Shumard (27) also reported a decrease in the digestibility of protein in ovine coccidiosis. A possible explanation for the increase in the digestion absorption of proteins during tre acute phase of E. acervulina infection (34) may be due to an increase in the protein and amino acid pool in the intestinal lumen caused by an increased permeability of intestinal mucosa for the passage of plasma proteins (4, 13, 20, 24). Intestinal coccidiosis has therefore been considered as a protein loosing enteropathy (11). That infection with E. acervulina in the acute phase decreased the protein retention in the chicken but increased the digestion absorption of proteins (34) suggests that coccidial infection only affects the postabsorptive protein metabolism of the host. This concept has found further support from the recent studies of Musajev and Surkova (17) who reported a decrease in the total and protein nitrogen in the liver of the chicken infected with E. tenella or E. mitis during days 3 to 5 postinfection. Larbier and Yvore (14) also observed an

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Infected 30.91 4.54 42.75 14 2.45 0.86 36.78 40.25 zh 1.46 28.55 4 2.32 34.60 i 3.10

Efficiency of Utilization of Dietary Metabolizable Energy for Tissue Deposition Control 27.66 i 10.7 28.70 i 0.90 26.04 i 1.92 28.90 i 6.10 28.39 i 0.83 32.75 i1 3.35

Infected 21.44 i 2.70 24.15 i 3.05 23.83 i 0.55 26.45 ±t 0.75 24.07 + 1.69 25.60 + 1.10

increase in the total free amino acids in the muscle but a decrease in the serum protein during the acute phase of E. acervulina infection. Infection with E. acervulina caused a marked reduction in the retention of ether extract with an increased loss of ether extract in the excreta which confirms the results of Turk and Stephens (35) who observed a decreased absorption of 1311.

labelled oleic acid during the acute phase of this infection. The present study indicates that infection with E. acervulitna also reduced the availability of the metabolizable energy to the chicken and increased the fecal energy loss. The decrease in the ME may be caused by a reduction in the digestion absorption of fat as observed in this study and to a reduction in the absorption of glucose (8, 33). The decreased availability of ME may be a major contributing factor in the decrease in protein synthesis as observed during the acute phase of this infection since the energetic cost of deposition of protein is very high (26). The results of the chemical composition of the carcass also suggests that the efficiency of utilization of the available ME to the chicken is reduced during the acute phase of E. acervulina. Sykes (32) also reported a decreased utilization of absorbed energy in this infection. Whether the decrease in the energetic efficiency lies at the level of maintenance and/or growth is not known. The resting oxygen consumption of the E. acervulina infected chickens was found to be depressed during the acute phase (31). Estimates of metabolizable energy of the feed ingredients have been used extensively in nutritional experiments and in practical diet formulations. The present study in-

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dicates that the ME value of the diet is decreased during the acute phase of E. acervulina infection. Infection with E. acervulina did not influence the retention of ash, calcium and phosphorus during the acute phase but increased the retention of the latter mineral during the recovery phase of the disease. That coccidial infection affects the mineral metabolism of the host is indicated by the report of Stafseth (29) who observed greater severity of rickets in chickens suffering from coccidiosis. Turk and Stephens (35) also observed a decreased rate of zinc absorption during the acute phase and an increase during the recovery phase of E. acervutlina infection. The precise mechanism of fat malabsorption in E. acervutlina infection is not clear. A similar clinical entity occurs in human coccidiosis caused by Isospora belli infection (1, 3, 7). Steatorrhea may result from an impairment of intraluminal hydrolysis or solubilization of fat, decreased uptake of the products of fat hydrolysis by the epithelial cells or to the abnormalities of mucosal cell transport (28). Infection with E. acervulina causes a reduction in the pH of the intestinal contents (12). An impairment in the hydrolysis of fat caused by increased intestinal acidity may occur as a result of irreversible destruction in the activity of pancreatic lipase as observed in Zollinger-Ellison syndrome in human subjects (9). However, impairment in the fat hydrolysis or the uptake of the products of fat hydrolysis by the epithelial cells may not be the major factor in fat malabsorption in this infection since the electron microscopic studies revealed the presence of fat within the epithelial cells. The present studies indicate that the metabolism of the epithelial cells is impaired as a result of parasitism. Fat droplets were observed only in villus epithelial cells parasitized by the gamonts of E. acerviulina. The accumulation of fat within the villus epithelial cells may be an indication of the immaturity of these cells since the rate of cell renewal of the crypt cells was found to be increased in this infection (6). The undifferentiated cells reaching the villus are not able to metabolize the accumulated fat since fat absorption is primarily a function of highly differentiated epithelial cells at the villus top only (38). The rate limiting step in the normal absorption of fat lies at the exit of fat from the intestinal cells (38).

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Steatorrhea in intestinal coccidiosis may therefore result from the extrusion of reconstituted fat globules after the rupture of the parasitized epithelial cells. The large amount of unabsorbed fat in the intestinal lumen may cause diarrhea with a loss of fluid and electrolytes possibly owing to bacterial production of C-18 fatty acids which may have irritant properties (39).

ACKNOWLEDGMENTS The senior author acknowledges the award of a postdoctoral fellowship of the Medical Research Council of Canada. This work was supported in part by the Ontario Ministry of Agriculture and Food and by the Ontario Ministry of Health. Thanks are due to Mr. Orvar Remmler of the Department of Pathology for his invaluable help throughout the course of experiments. REFERENCES 1. AMENT, M. E. Malabsorption syndromes in infancy and childhood. Part I. J. Pediatrics. 81: 685-697. 1972. 2. Association of Official Agricultural Chemists. Official methods of analysis. 10th edition. Washington, D.C. 1965. 3. BRANDBORG, L. L., S. B. GOLDBERG and W. C. BREIDENBACH. Human coccidiosis. A possible cause of malabsorption. New Engl. J. Med. 283: 1306. 1970. 4. ENIGK, K., H. SCHANZEL, E. SCUPIN and A. DEY-HAZRA. Intestinal protein loss in avian coccidiosis. Zentbl. VetMed. 17 B: 522-526. 1970. 5. FERNANDO, M. A. Fine structure of the schizonts and merozoits of Eimeria acervulina in the chicken. J. Parasit. 60: 149-159. 1974. 6. FERNANDO, M. A. and B. M. McCRAW. Mucosal morphology and cellular renewal in the intestine of chickens following a single infection of Eimeria acervulina J. Parasit. 59: 493-501. 1973. 7. FRENCH, J. M., J. L. WHITBY and A. G. W. WHITFIELD. Steatorrhea in a man infected with coccidiosis (Isospora belli). Gastroenterology 47: 642. 1964. 8. GIESE, W., V. STOLL, A. DEY-HAZRA and K. ENIGK. Der Einfluss verschiedener Eimeria-Arten auf absor-ption und Stoffwechsel von 14C-glucose bei Huhnerkuken. Expl Parasit. 29: 440-450. 1971. 9. GO, V. L. W., J. R. POLEY, A. F. HOFMANN and W. J. H. SUMMERSKILL. Abnormalities of fat digestion in ulcerogenic islet cell tumor with steatorrhea. Gastroenterology 54: 1239. 1970. 10. HEIN, M. The pathogenic effects of Eimeria acervulina in young chicks. Expl Parasit. 22: 1-11. 1968. 11. KOUWENHOVEN, B. Eimeria avervulina infection in chickens; a parasitological and biochemical study (summary). Neth. vet. J. 4: 112-114. 1971. 12. KOUWENHOVEN, B. and C. J. G. VAN DER HOST. Strongly acid intestinal content and lowered protein, carotene and vitamin A blood levels in Eimeria acervulina infected chickens. Z. ParasitKde 32: 347-353. 1969. 13. KOUWENHOVEN, B. and C. J. G. VAN DER HOST. Significance and possible cause of the lowered intestinal pH during Eimeria acervulina infection in the fowl. II. Int. Congr. Parasit. J. Parasit. 56: (4) Section II, part I. 191-192. 1970.

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Can. J. comp. Med.

Effect of Eimeria acervulina infection on nutrient retention with special reference to fat malabsorption in chickens.

Effect of Eimeria acervulina Infection on Nutrient Retention with Special Reference to Fat Malabsorption in Chickens V. D. Sharma and M. A. Fernando*...
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