| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
METABOLISM AND NUTRITION |
* Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Science, Shiqiao Road, Hangzhou, P. R. China, 310021; Parasitology Laboratory, College of Veterinary Medicine, China Agriculture University, Beijing 100094, China; China National Feed Quality Control Centre, Zhongguancun Nan Road, Haidian District, Beijing, P. R. China, 100081; and Hangzhou Academy of Agriculture Science, Hangzhou, P. R. China, 310024
1 Corresponding author: xxww101{at}sina.com
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Key Words: proanthocyanidin • growth • chicken • Eimeria • antioxidant
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Avian protozoa, such as Eimeria, are one of the leading causes of poultry disease, and responsible for major economic losses in poultry industry by increasing mortality and reducing growth rates (Guo et al., 2007). The generation of proinflammatory mediators, together with the oxidative and nitrous oxide species, contributed principally to inflammatory injury and diarrhea. As occurred mostly in the case of parasite infection, the enzymatic antioxidant system of chicken, including superoxide dismutase (SOD) and catalase (CAT), was significantly decreased when infected with Eimeria tenella (Georgieva et al., 2006). Changes in concentrations of serum NO and carotenoid were also detected with chicken coccidiosis (Allen, 1997), which suggested that the unbalanced oxidant/antioxidant status is likely to be important in the progress of disease (Georgieva et al., 2006). Therefore, substances that generate oxidative stress [e.g., artemisnin (Allen et al., 1997)] or have antioxidant properties, such as n-3 fatty acids, 
-tocopherol, curcumin, and green tea extracts, demonstrated certain coccidiastat effects (Allen et al., 1996; Allen and Danforth, 1998; Guo et al., 2004; Jang et al., 2007). The common approaches used in the last decade for the control of avian coccidiosis relied heavily on anticoccidial feed additives, which increased the resistance of the parasite to the traditional coccidacidal pharmaceuticals and consequently led to the ban of chemotherapeutic methods. Therefore, there is an increasing demand for new antioxidant and immunological prophylaxis.
The objective of the present experiment was to investigate the effect of dietary condensed tannin, which was isolated from grape seeds, on the performance of broilers chickens after coccidiosis infection. Because proanthocyanidin has superior antioxidant properties, the influences of dietary proanthocyanidin on oxidative stress-related parameters were also evaluated.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Grape seed proanthocyanidin extract, which was extracted from grape seed with the ethanol method, was purchased from Jianfeng Natural Products Co. Ltd. (Tianjing, China). The concentration of proanthocyanidin compound determined by UV Bate-Smith colorimetric method was 98.14% (Bate-Smith, 1975). The composition of GSPE is 10% of monomer, 61.32% of oligomer with degree of polymerization between 2 to 5, and 28.68% of polymers, which was checked by HPLC (Pekic et al., 1998). Unless indicated otherwise, all other chemicals and reagents were purchased from Sigma-Aldrich Co. (St. Louis, MO).
Birds and Experimental Design
Experiment 1.
To evaluate the effect of dietary GSPE on the performance of broiler chickens after E. tenella infection, a total of 216 one-day-old as-hatched Shiqizha broiler chickens of both sexes were obtained from a local hatchery (Institute of Animal Science of China Academy of Agricultural Sciences, Beijing, China). They were weighed individually, labeled with feet-ring, and allotted to 8 treatments with 3 replicated cages of 10 birds each. A plastic sheet was placed under the cage to collect excreta, and the sheet was changed daily. All chicks were free from coccidian infection and commercial vaccinations. The mean BW difference between each cage was less than 1 g at d 1. Birds in treatment 1, 2, 3, 4, 5 were fed the diets contained 5, 10, 20, 40, and 80 mg/kg of GSPE, respectively, from d 1. Treatments 6 and 7 were assigned to salinomycin (66 mg/kg, Qilu Kingphar Pharmaceutical Co. Ltd., Shandong, China) and maduramicin ammonium treatment (5 mg/kg, Cygro premix, Alpharma Inc., Bridgewater, NJ) respectively. Infected and noninfected controls were assigned as treatments 8 and 9, respectively. Chicks were brooded initially at 31 to 33°C in the first 5 d and with following weekly reduction of 2 to 3°C until the temperature reached 22 to 23°C. Lighting was continuous and the relative humidity was 60%. Maize and soybean-based starter diets, without any antibiotic additives, were formulated based on the Feeding Standard of Chickens in China (NY-T 33-2004; Table 1
), and provided ad libitum to all birds with water. At d 8, all treatments except noninfected control were inoculated with 5 x 104 sporulated oocysts by oral gavage. Body weight gain, mortality, and excreta conditions were recorded daily after oocyst infection.
|
). There were 3 replicate cages assigned into each treatment, and a total of 7 treatments were included in the current experiment. Birds in treatments 1, 2, and 3 were fed diet formulated to contain 12 mg/kg of GSPE, whereas birds in the rest of the treatments were fed a similar diet without any supplement. All experimental birds except noninfected controls (treatment 7) were challenged with different dosage of E. tenella oocysts at 14 d of age by oral gavage. Birds in treatments 1 and 4 were infected by 1 x 105 sporulated oocysts, and those in treatments 2 and 5 were inoculated by 5 x 104 oocysts, whereas 1 x 104 oocysts were given to birds in treatments 3 and 6 respectively. All the birds used in the experiment were treated in strict compliance with the current regulation concerning laboratory animals of China and approved by the laboratory animal care and usage committee, Zhejiang Academy of Agricultural Science.
Parasites Preparation
The E. tenella strain used in the current experiment was provided by the Parasitology Laboratory, College of Veterinary Medicine, China Agricultural University (the E. tenella Houghton strain, described by Chapman and Shirley, 2003). It was maintained by periodic passage through coccidia-free chickens, and those unsporulated oocysts obtained from the cecum contents on d 7 postinoculation were purified and processed by standard operation. The degree of sporulation and oocysts population was enumerated by microscopy according to the procedure of Suo and Li (1998) before challenge.
Sampling and Data Collection
In experiment 1, BW of each bird was weighed on d 1, 8, and 15. Mortality was recorded daily. At the end of the experiment (d 15), each bird was weighed, identified according to the treatment, anesthetized, and killed by cervical dislocation. The intestine was removed and opened. The lesion scores ranging from 0 (no gross lesion) to 4 (most severe gross lesion) in the appropriate regions were recorded (Johnson and Reid, 1970). For oocyst output determination, total fecal output of each cage at d-7 postinfection was weighed, and oocyst output was determined from duplicate counts (Long and Joyner, 1976).
In experiment 2, birds from each treatment were weighed individually on d 1, 14, and 21. At d 21, blood samples were randomly collected by cardiac puncture from 3 chickens of each replicate, and 9 total blood samples were obtained. Four milliliters of whole blood was taken from each chicken and mixed with 400 µL (16.5 mg/mL) of EDTA, which was previously placed into the test tube. The mixture was centrifuged at 2,500 x g at 4°C for 15 min to collect the plasma and stored –20°C until use. Then the bird was anesthetized with ether and killed by cervical dislocation. Mucosal samples from the end of duodenum to the ileocecal junction of 9 chickens (3 broilers of each replicate) were also scraped off by using microscope slides, frozen in liquid nitrogen, and kept at –80°C. The ceca of bird were removed and opened. The lesions scores in the appropriate regions were recorded (Johnson and Reid, 1970).
Samples Analysis
Plasma NO Assay. The total concentration of NO2– + NO3– in plasma from experiment 2 was determined and expressed as the plasma NO concentration as described by Allen (1997). Nine plasma samples randomly selected from each treatment of 3 cages were analyzed for NO concentration. In brief, total NO2– + NO3– in 100-µL aliquots of rapid thawed plasma was determined by reducing NO3– to NO2– with nitrate re-ductase. The total NO2– was measured colorimetrically by the absorbance at 550 nm. The concentration of NO was expressed as µmole per liter of plasma. The assay was conducted using a kit (Cat. No. A012, NO2–+NO3–) purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, China).
Mucosal NO Assay. Nine rapid-thawed mucosal samples were quickly homogenized to make 10% homogenates with ice-cold PBS, then centrifuged at 1,000 x g at 4°C for 30 min to collect the supernatant. Total NO2– + NO3– in 100-µL aliquots of supernatant were measured using nitrate reductase kit (Cat. No. A012, NO2– + NO3–) purchased from Nanjing Jiancheng Bio-engineering Institute (Nanjing, China).
Determination of Plasma Superoxide Dismutase Activities
The SOD activities of plasma samples in experiment 2 were assayed based on the ability of SOD to inhibit the reduction of nitroblue tetrazolum by superoxide (Worthington, 1993). Nine plasma samples randomly selected from each treatment (3 chicks of each cage from 3 cages) were analyzed; 1 unit of SOD is defined as the amount of sample resulting in 50% inhibition of nitroblue tetrazolum reduction. Results of SOD activities were expressed as unit per milliliter of plasma. The enzyme activity was measured using a kit (Cat. No. A001–1 SOD) purchased from Nanjing Jiancheng Bioengineering Institute (Nanjing, China).
Determination of Plasma Malondiadehyde
The concentrations of malondialdehyde (MDA) in plasma of experiment 2 were determined by the method described by Ohkawa et al. (1979). A 100-µL aliquot of plasma was mixed with thiobarbituric acid reagent and incubated. After centrifugation, the optical density of the clear pink supernatant was read at 532 nm. Malondialdehyde bis (dimethyl acetal) was used as standard. The assay was conducted using a kit (Cat. No. A003–1, MDA) purchased from Nanjing Jiancheng Bio-engineering Institute (Nanjing, China).
Determination of Total Protein
The protein concentrations of mucosal samples were determined by the method of Lowry et al. (1951). Bovine serum albumin was used as a standard.
Statistical Analysis
In experiment 2, three different enzyme activities were determined. Values are reported as the means with their SEM. For calculation of bird BW, the experimental unit was the mean of BW for each cage of birds. The significance of differences between means was determined by ANOVA procedure of SPSS version 13.0 software (SPSS Inc., Chicago, IL). Value (P 
0.05) was considered significant.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The effect of different concentrations of dietary GSPE on the BW gain in experiment 1, which was calculated before and after infection, was shown in Table 2. From d 1 to 8, BW gain was not affected by treatments. After infection with 5 x 104 oocysts of E. tenella, weight gain was reduced in all groups except those fed maduramicin, indicating the sufficient effectiveness of maduramicin against E. tenella Houghton strain. Furthermore, birds in all GSPE-treated groups had significantly greater BW (P < 0.05) than infected control after infection. In general the average weight gains in GSPE treatments were similar to salinomycin treatment and significantly greater than infected control for the entire experimental duration.
|
. The average BW gains in groups supplemented with GSPE were slightly greater than non-supplemented groups, which was consistent with the observation from experiment 1. During the period of Eimeria infection (d 14 to 21), the BW gains were significantly influenced by the infection dosage of E. tenalla regardless of the dietary formulation. The lowest weight gains were recorded in groups infected with 1 x 105 of oocysts. Again, incorporation of 12 mg/kg of GSPE significantly increased BW gains in comparison with the control after the infection. The best BW gains were obtained from the noninfected group.
|
Death occurred in both experiments after E. tenella infection. The mortality in the infected control group was 46% in experiment 1. In groups of maduramicin, GSPE 10 mg/kg and salinomycin treatments, the mortalities were 3.3, 6.7, and 10%, respectively (Table 3). In general increase of dietary GSPE over 20 mg/kg had a deleterious effect on the live performance criteria such as weight gains and mortalities. In experiment 2, there was no occurrence of death in GSPE-treated groups, in contrast, 27% mortalities occurred in the control treatments 4 and 5, when 1 x 105 and 5 x 104 oocysts were inoculated (Table 4).
|
for experiment 1, lesion scores were significantly improved in all GSPE-treated groups in comparison with infected control and similar scores to the salinomycin group. The lowest lesion score was recorded in the maduramicin group. For experiment 2, cecal lesion scores are presented in Table 4. Incorporation of 12 mg/kg of GSPE into the diet significantly decreased the lesion scores in the cecum, particularly with severe infection (5 x 104 and 1 x 105 dosage).
Fecal oocyst outputs in experiment 1 were determined on d 7 postinfection. As demonstrated in Table 3, number of oocysts decreased in all GSPE-treated groups in comparison with infected control and showed a similar level to the salinomycin group. Furthermore, there were no oocysts detected in the maduramycin group. For experiment 2, fecal oocysts output was enumerated at d 5, 6, and 7 postinfection. In general the incorporation of 12 mg/kg of GSPE did not show a remarkable effect on the number of oocysts in feces.
Daily fecal weight was significantly reduced from 20.31 to 11.96 g/bird at d 5 postinfection at the greatest infection dose. In contrast the fecal weight from the group supplemented with 12 mg/kg of GSPE was 22.81 g/bird (Table 5). At d 7, the fecal outputs from all infected groups were increased due to the expected increased gut inflammation and possible edema formation. The fecal output from the uninfected control group from d 1 to 7 remained relatively unchanged.
|
The concentrations of plasma NO2– + NO3– at d 8 postinfection in experiment 2 showed a statistically significant increase (P 0.05; Table 6). The magnitude of increase seems to be influenced by the infectious dose (e.g., from 11.06 to 22.82 µmol/L when the infectious dose elevated from 1 x 104 to 5 x 104, respectively). Diets supplemented with GSPE significantly decreased the mean level of plasma NO2– + NO3– from 21.31 to 14.73 µmol/L in the group of birds infected with high dose (P 0.05). For mucosal samples, the concentration of NO declined after the infection of E. tenella. In contrast, NO level in mucosal significantly elevated when GSPE was incorporated into the diets.
|
As demonstrated in Table 6, the plasma SOD activities decreased to 111.14 U/L when the birds were infected with the greatest dose of 1 x 105 of E. tenella; however, the uninfected group showed a level of 126.55 U/L. The plasma MDA also increased from 0.91 to 1.49 µmol/L (P 0.05), indicating the occurrence of oxidative stress. Adding GSPE into chicks’ diets significantly elevated plasma SOD from 111.14 to 133.27 U/L (P 0.05) and decreased the plasma MDA level. At the lower infecting dose (<5 x 104), the GSPE effect appears to be less obvious.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Grape seed proanthocyanidins are natural polyphenolic compounds widely distributed in greater plants and have been utilized as special food supplements in human diets for many years. The interests in application of those compounds to human nutrition recently accelerated due to the accumulated evidence demonstrating that GSPE are the first and foremost powerful multifunction antioxidants with free radical scavenging activity and transition metal chelating activity (Cos et al., 2003). Furthermore, it has been also reported that proanthocyanidin was a potent inhibitor of the pro-inflammatory cytokine and chemokine responses induced by lipopolysaccharides (Bodet et al., 2006), and as a consequence the anti-inflammatory effect is capable of prolonging the life span of mice infected by Trichomonad (Tomobe et al., 2007). Those previous data with mice were consistent with our current results. Supplementation of GSPE significantly decreased the severity of cecal lesions and mortality of birds as well as increasing BW gains and daily fecal weight, suggesting that the proanthocyanidins in grape seed extracts exerted an anti-inflammatory impact against the E. tenella infection. However, the beneficial effect was in a dose-dependent manner because the lowest mortality was only observed in the group fed with 10 mg/kg of GSPE and the death accelerated along with increase of concentration of GSPE. Those results indicated that overdosed GSPE may exert a potential detrimental impact. Thus, as many other plant extracts, GSPE has been shown to play a double-edged role in the regulation of inflammatory system of the host, and caution in intake dosage should be carefully taken to avoid switching over from beneficial effects to adverse ones.
In the current experiment, plasma levels of nitric oxide on d 8 after infection with E. tenella increased in a dose-dependent manner. As reported by previous study, those results suggested cell-mediated immune response has been activated (Allen, 1997; Allen and Lillehoj, 1998). Although it is still unclear on whether increased level of plasma NO caused by infection of E. tenella was due to either inducible nitric oxide synthase or constitutive NOS (Nie et al., 2004), it has been agreed that increased plasma NO after E. tenella challenge was intimately involved in a normal pathological process and is of significance in defending against parasite infection. It has been reported that exogenous NO is toxic to sporulated oocysts (Yan et al., 2005), and when NOS inhibitors (e.g., L-Aminoguanidi and NG-monomethyl- L-arginine) were ingested by the birds after the E. tenella infection, the feacal oocyst outputs were slightly increased (Allen and Lillehoj, 1998; Shen et al., 2002). However, high concentration of NO and free radicals generated by the host may be over the threshold of cell tolerance causing the tissue damage and cytotoxicity (Evans and Halliwell, 2001), which partly contributed to the development of inflammatory symptoms such as diarrhea, mortality, and weight loss. It seemed that after parasite invasion, free radicals, together with the high level of NO production, were the major factors that compromised the cellular anti-oxidant defense system (Georgieva et al., 2006). In current study, the decreased activities of plasma SOD as well as increased level of MDA (Table 6), as reported previously, implied an imbalanced status of oxidants/ antioxidants occurred and oxidative stress accumulated (Sundaram et al., 2003; Georgieva et al., 2006). Therefore, compounds that are meeting the demands of antioxidant defense system or directly interfere with free radicals, such as GSPE, will restore the balance of oxidants/antioxidants, leading to improvement of growth performance.
Numerous results accumulated regarding the mechanism of GSPE in health promotion and disease prevention. However, the mode of action is complex due to the dose-dependent scavenging capacity of the free radicals and the regulation of NO production (Bagchi et al., 2000; Shao et al., 2006; Wang et al., 2006). The latter can be due to the enhancement of NO production or due to the downregulation of NO production depending on the type of cell, location, and timing (Wang et al., 2006). The GSPE increased NO production with chick cardiomyocyte in a dose-dependent manner, leading to severe cytotoxicity and cell apoptosis at the concentration of GSPE over 0.5 mg/mL (Shao et al., 2006). In contrast GSPE significantly inhibited NO production from macrophage RAW264.7, resulting in the decline of inflammation of tissues (Wang et al., 2006). In the current experiment, the level of plasma NO significantly decreased from 21 to 14 µM and mucosal NO slightly increased from 2.81 to 4.35 nmol/mg of protein when 12 mg/kg of GSPE was incorporated into the diet, suggesting that plasma and mucosal NO are produced by different types of cells and modulated by GSPE in different regulation systems. Further investigation was conducted for the mechanisms involved in the regulation of NO production by GSPE in plasma and mucosal after parasite infection. Additionally, due to the coccidiocidal effects of NO, the decreased NO concentration in plasma and the slight increase in mucosa may explain the fact that there were nonsignificant impacts in the fecal oocyst output after incorporation of GSPE into the diet.
In conclusion, the results presented in current study demonstrated that incorporation of GSPE as low as 10 to 20 mg/kg is able to enhance the growth performance of broilers and significantly reduce the mortality of chicks after the E. tenella infection. Results of increased plasma SOD contents, decreased MDA, and plasma NO concentration suggested GSPE, the strongest antioxidant reagent, was able to restore the balance of oxidant-antioxident status, which was disturbed by the parasite infection through oxidative stress. Because dietary antioxidants have long been associated with the susceptibility to infectious disease (Beck, 2001; Horak et al., 2006), much more work is needed on the elaboration of low concentrations of condensed tannins (e.g., GSPE) in the application of animal nutrition.
Received for publication February 20, 2008. Accepted for publication July 14, 2008.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Allen, P. C., and H. D. Danforth. 1998. Effects of dietary supplementation with n-3 fatty acid ethyl esters on coccidiosis in chickens. Poult. Sci. 77:1631–1635.
Allen, P. C., H. D. Danforth, V. L. Morris, and O. A. Levander. 1996. Association of lowered plasma carotenoids with protection against cecal coccidiosis by diets high in n-3 fatty acids. Poult. Sci. 75:966–973.[Web of Science][Medline]
Allen, P. C., and H. S. Lillehoj. 1998. Genetic influence on nitric oxide production during Eimeria tenella infections in chickens. Avian Dis. 42:397–403.[CrossRef][Web of Science][Medline]
Allen, P. C., J. Lydon, and H. D. Danforth. 1997. Effects of components of Artemisia annua on coccidia infections in chickens. Poult. Sci. 76:1156–1163.
Bagchi, D., M. Bagchi, J. S. Stohs, K. D. Das, S. D. Ray, C. A. Kuszynski, S. S. Joshi, and H. G. Pruess. 2000. Free radical and grape seed proanthocyanidin extract: Importance in human health and disease prevention. Toxicology 148:187–197.[CrossRef][Web of Science][Medline]
Bate-Smith, E. C. 1975. Phytochemistry of proanthocyanidins. Phytochemistry 14:1107–1113.[CrossRef][Web of Science]
Bate-Smith, E. C., and T. Swain. 1962. Flavonoid compounds. Pages 705–809 in Comparative Biochemistry. H. S. Mason and A. M. Florkin, ed. Academic Press, New York, NY.
Beck, M. A. 2001. Antioxidants and viral infections: Host immune response and viral pathogenicity. J. Am. Coll. Nutr. 20:384S–388S.
Bodet, C., F. Chandad, and D. Grenier. 2006. Anti-inflammatory activity of a high-molecular-weight cranberry fraction on macrophages stimulated by lipopolysaccharides from periodontopathogens. J. Dent. Res. 85:235–239.
Calzada, F., C. M. Cerda-Garcia-Rojas, M. Meckes, R. Cedil-lo-Rivera, R. Bye, and R. Mata. 1999. Geranins A and B, new anti-protozoal A-type proanthocyanidins from Geranium niveum. J. Nat. Prod. 62:705–709.[CrossRef][Medline]
Calzada, F., R. Cedillo-Rivera, R. Bye, and R. Mata. 2001. Geranins C and D, additional new antiprotozoal A-type proanthocyanidins from Geranium niveum. Planta Med. 67:677–680.[CrossRef][Web of Science][Medline]
Chapman, H. D., and M. W. Shirley. 2003. The Houghton strain of Eimeria tenella: A review of the type strain selected from genome sequencing. Avian Pathol. 32:115–127.[CrossRef][Web of Science][Medline]
Cos, P., N. De Bruyne, S. Hermans, D. Apers, V. Berghe, and A. J. Vlietink. 2003. Proanthocyanidins in health care current and new trends. Curr. Med. Chem. 10:1345–1359.
Evans, P., and B. Halliwell. 2001. Micronutrients: Oxidant/ antioxidant status. Br. J. Nutr. 85(Suppl.2):S67–S74.[Web of Science][Medline]
Georgieva, N. V., V. Koinarski, and V. Gadjeva. 2006. Anti-oxidant status during the course of Eimeria tenella infection in broiler chickens. Vet. J. 172:488–492.[CrossRef][Web of Science][Medline]
Guo, F. C., X. Suo, G. Z. Zhang, and J. Z. Shen. 2007. Efficacy of decoquinate against sensitive laboratory strains of Eimeria tenella and field isolates of Eimeria spp in broiler chickens in China. Vet. Parasitol. 147:239–245.[CrossRef][Web of Science][Medline]
Guo, F. C., R. P. Kwakkel, B. A. Williams, H. K. Parmentier, W. K. Li, Z. Q. Yang, and M. W. A. Verstegen. 2004. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella–infected chickens. Poult. Sci. 83:1124–1132.
Horak, P., M. Zilmer, L. Saks, I. Ots, U. Karus, and K. Zilmer. 2006. Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J. Exp. Biol. 209:4329–4338.
Jang, S. I., M. Jun, H. S. Lillehoj, R. A. Dalloul, I. K. Kongmn, S. Kim, and W. Min. 2007. Anticoccidial effect of green tea-based diets against Eimeria maxima. Vet. Parasitol. 144:172–175.[CrossRef][Web of Science][Medline]
Johnson, J., and W. M. Reid. 1970. Anticoccidial drugs: Lesion scoring techniques in battery and floor pen experiments with chickens. Exp. Parasitol. 28:30–36.[CrossRef][Web of Science][Medline]
Long, P. L., and L. P. Joyner. 1976. A guide to laboratory techniques used in the study and diagnosis of avian coccidiosis. Folia Vet. Lat. 6:201–217.[Medline]
Lowry, O. H., N. J. Rosenbrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193:265–275.
Muzitano, M. F., L. W. Tinoco, C. Guette, C. R. Kaiser, B. Rossi-Bergmann, and S. S. Costa. 2006. The antileishmanial activity assessment of unusual flavonoids from Kalanchoe pinnata. Phytochemistry 67:2071–2077.[CrossRef][Web of Science][Medline]
Nie, K., S. J. Hu, X. F. Zhou, R. H. Tang, and Y. Liu. 2004. Dynamic changes of activity of nitric oxide syntheses in sera and some organs of chickens infected with Eimeria tenella. Acta. Parasitol. Med. Entomol. Sin. 11:11–15.
Ohkawa, H., N. Ohishi, and K. Yagi. 1979. Assay of lipid per-oxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351–358.[CrossRef][Web of Science][Medline]
Pekic, B., V. Kovac, E. Alonso, and E. Revilla. 1998. Study of the extraction of proanthocyanidins from grape seeds. Food Chem. 61:201–206.[CrossRef]
Rapport, L., and B. Lockwood. 2001. Proanthocyanidins and grape seed extract. Pharm. J. 266:581–584.
Shao, Z. H., C. W. Hsu, and W. T. Chang. 2006. Cytotoxicity induced by grape seed proanthocyanidins: Role of nitric oxide. Cell Biol. Toxicol. 66:149–158.
Shen, Z. J., B. L. Zhu, and J. S. Jiang. 2002. The effect of NO during E. tenella or E. acervulina infection of broilers. Acta Vet. Zootech. Sin. 33:395–399.
Shi, J., J. Yu, J. E. Pohorly, and Y. Kakuda. 2003. Polyphenolics in grape seeds—biochemistry and functionality. J. Med. Food 6:291–299.[CrossRef][Medline]
Shimada, K., H. Watanabe, K. Hosoda, K. Takeuchi, and J. Yoshikawa. 1999. Effect of red wine on coronary flow-velocity reserve. Lancet 254:1002.
Sundaram, U., H. Hassanain, Z. Suntres, J. G. Yu, H. J. Cooke, J. Guzman, and F. L. Christofi. 2003. Rabbit chronic ileitis leads to up-regulation of adenosine A1/A3 gene products, oxidative stress, and immune modulation. Biochem. Pharmacol. 65:1529–1538.[CrossRef][Web of Science][Medline]
Suo, X., and G. Q. Li. 1998. The diagnosis for chicken coccidiosis. Pages 256–257 in Coccidia and Coccidiosis of Domestic Fowl (in Chinese). X. Suo, ed. China Agriculture University Press, Beijing.
Tomobe, K., H. Fujii, B. Sun, H. Nishioka, and O. I. Aruoma. 2007. Modulation of infection-induced inflammation and locomotive deficit and longevity in senescence-accelerated mice-prone (SAMP8) model by the oligomerized polyphenol oligonol. Biomed. Pharmacother. 61:427–434.[CrossRef][Medline]
Waghorn, G. C., and W. C. McNabb. 2003. Consequences of plant phenolic compounds for productivity and health of ruminants. Proc. Nutr. Soc. 62:383–392. (Review).[CrossRef][Web of Science][Medline]
Wang, X. G., T. Liang, and K. Y. Zhou. 2006. Effects of proanthocyanidins on the expression of induced nitric oxide synthase (iNOS) gene in peritoneal macrophage of rats with adjuvant arthritis. J. China Pharm. Univ. 37:263–267.
Worthington, V. 1993. Superoxide Dismutase. Pages 368–369 in Worthington Enzyme Manual. N. J. Freehold, ed. Worthington Biochemical Corp., Lakewood, NJ.
Yamakoshi, J., S. Kataoka, T. Koga, and T. Ariga. 1999. Proanthocyanidin-rich extract from grape seeds attenuates the development of aortic atherosclerosis in cholesterol-fed rabbits. Atherosclerosis 142:139–149.[CrossRef][Web of Science][Medline]
Yan, J. Y., H. X. Zhang, J. G. Li, and J. P. Tao. 2005. Effects of exogenous nitric oxide on Eimeria tenella in chickens. Guangxi J. Anim. Husbandry Vet. Med. 36:6–8. (in Chinese).
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
