Consumption of Agaricus bisporus mushroom affects the performance, intestinal microbiota composition and morphology, and antioxidant status of turkey poults

Animal Feed Science and Technology

Volumn 165, Issue 3-4, 2011, Pages 218-229

  Giannenas, I ^a   Tsalie, E ^a   Chronis, E ^b   Mavridis, S ^a   Tontis, D ^a   Kyriazakis, I ^a  

^a UNIVERSITY OF THESSALY   (Greece)

^b 3rd Military Veterinary Hospital   (Greece)

Author keywords

Agaricus bisporus; Antioxidant activity; Growth; Intestinal bacteria; Intestinal morphology; Turkey

Indexed keywords

AGARICUS BISPORUS; AVES; BACTEROIDES; BACTEROIDES SP.; BASIDIOMYCOTA; BIFIDOBACTERIUM; ENTEROCOCCUS; ESCHERICHIA COLI; LACTOBACILLUS; MELEAGRIS GALLOPAVO;

EID: 79955470045     PISSN: 03778401     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anifeedsci.2011.03.002     Document Type: Article

References (63)

1. AOAC International Official Methods of Analysis of AOAC International 1995, AOAC Int., Arlington, VA, USA. sixteenth ed.
2. Apajalahti J., Kettunen A., Graham H. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poult. Sci. J. 2004, 60:223-232.
3. Botsoglou N.A., Florou-Paneri P., Christaki E., Fletouris D.J., Spais A.B. Effect of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues. Br. Poult. Sci. 2002, 43:223-230.
4. Botsoglou N.A., Papageorgiou G., Nikolakakis I., Florou-Paneri P., Giannenas I., Dotas V., Sinapis E. Effect of dietary dried tomato pulp on oxidative stability of Japanese quail meat. J. Agric. Food Chem. 2004, 52:2982-2988.
5. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein, utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-252.
6. Breene W.M. Nutritional and medicinal value of specialty mushrooms. J. Food Prot. 1990, 53:883-894.
7. Buege J.A., Aust S.T. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
8. Chang S.T., Buswell J.A. Mushroom nutriceuticals. World's J. Microbiol. Biotechnol. 1996, 12:473-476.
9. Cheung L.M., Cheung P.C.K., Ooi V.E.C. Antioxidant activity and total phenolics of edible mushroom extracts. Food Chem. 2003, 81:249-255.
10. Christaki E., Florou-Paneri P., Giannenas I., Papazahariadou M., Botsoglou N.A., Spais A.B. Effect of a mixture of herbal extracts on broiler chickens infected with Eimeria tenella. Anim. Res. 2004, 53:137-144.
11. Cook R.H., Bird F.H. Duodenal villus area and epithelial cellular migration in conventional and germ-free chicks. Poult. Sci. 1973, 52:2276-2280.
12. Dalloul R.A., Lillehoj H.S. Poultry coccidiosis. Recent advancements in control measures and vaccine development. Exp. Rev. Vaccines 2006, 5:143-163.
13. Dalloul R.A., Lillehoj H.S., Lee J.S., Lee S.H., Chung K.S. Immunopotentiating effect of a Fomitella fraxinea-derived lectin on chicken immunity and resistance to coccidiosis. Poult. Sci. 2006, 85:446-451.
14. Dubois M.K., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956, 28:350-356.
15. Dubost N.J., Ou B., Beelman R.B. Quantification of polyphenols and ergothioneine in cultivated mushrooms and correlation to total antioxidant capacity. Food Chem. 2007, 105:727-735.
16. European Commission Regulations, 1998. Amending Withdrawal of the Authorization of Certain Antibiotics. Amending Council Directive 70/524/EC Concerning Additives in Feedingstuffs (EC) No. 2821/98 of 17 December 1998 OJ L 351/4, pp. 1-5.
17. Fu H.Y., Shieh D.E., Ho C.T. Antioxidant and free radical scavenging activities of edible mushrooms. J. Food Lipids 2002, 9:35-46.
18. Giannenas I., Pappas I.S., Mavridis S., Kontopidis G., Skoufos J., Kyriazakis I. Performance and antioxidant status of broiler chickens supplemented with dried mushrooms (Agaricus bisporus) in their diet. Poult. Sci. 2010, 89:303-311.
19. Giannenas I., Tontis D., Tsalie E., Chronis Ef., Doukas D., Kyriazakis I. Influence of dietary mushroom Agaricus bisporus on intestinal morphology and microflora composition in broiler chickens. Res. Vet. Sci. 2010, 89:78-84.
20. Gibson G.R., Wang X. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J. Appl. Bacteriol. 1994, 77:412-420.
21. Guo, F.C., 2003. Mushroom and Herb Polysaccharides as Alternatives for Antimicrobial Growth Promoters in Poultry. Ph.D. Thesis. Wageningen University, The Netherlands.
22. Guo F.C., Kwakkel R.P., Williams B.A., Parmentier H.K., Li W.K., Yang Z.Q., Verstegen M.W.A. Effects of mushroom and herb polysaccharides on cellular and humoral immune responses of Eimeria tenella-infected chickens. Poult. Sci. 2004, 83:1124-1132.
23. Guo F.C., Williams B.A., Kwakkel R.P., Li H.S., Li X.P., Luo J.Y., Li W.K., Verstegen M.W.A. Effects of mushroom and herb polysaccharides, as alternatives for an antibiotic, on growth performance of broilers. Br. Poult. Sci. 2004, 45:684-694.
24. Guo F.C., Savelkoul H.F.J., Kwakkel R.P., Williams B.A., Verstegen M.W.A. Immunoactive, medicinal properties of mushroom and herb polysaccharides and their potential use in chicken diets. World's Poult. Sci. J. 2003, 59:427-440.
25. Habig W.H., Pabst M.J., Jakoby B.W. Glutathione s-transferase. The first enzymatic step in mercapturic acid formation. Biol. Chem. J. 1973, 249:7130-7139.
26. Hirano R., Sasamoto W., Matsumoto A., Itakura H., Igarashi O., Kondo K. Antioxidant ability of various flavonoids against DPPH radicals and LDL oxidation. J. Nutr. Sci. Vitaminol. 2001, 47:357-362.
27. Jamroz D., Orda J., Kamel C., Wiliczkiewicz A., Wertelecki T., Skorupinska J. The influence of phytogenic extract on performance, nutrients digestibility, carcass characteristic and gut microbial status in broiler chickens. J. Anim. Feed Sci. 2003, 12:583-596.
28. Jiang Z.Y., Jiang S.Q., Lin Y.C., Xi P.B., Yu D.Q., Wu T.X. Effects of soybean isoflavone on growth performance, meat quality, and antioxidation in male broilers. Poult. Sci. 2007, 86:1356-1362.
29. Jin L.Z., Ho Y.W., Abdullah N., Jalaludin S. Growth performance, intestinal microbial populations, and serum cholesterol of broilers fed diets containing Lactobacillus cultures. Poult. Sci. 1998, 77:1257-1265.
30. Juskiewicz J., Jankowski J., Zdunczyk Z., Biedrzycka E., Koncicki A. Performance and microbial status of turkeys fed diets containing different levels of inulin. Arch. Geflugel. 2005, 69(4):175-180.
31. Lo K.M., Cheung P.C.K. Antioxidant activity of extracts from the fruiting bodies of Agrocybe aegerita var. alba. Food Chem. 2005, 89:533-539.
32. Lopez-Bote C.J., Gray J.I., Gomaa E.A., Flegal C.G. Effect of dietary administration of oil extracts from rosemary and sage on lipid oxidation in broiler meat. Br. Poult. Sci. 1998, 39:235-240.
33. Manzi P., Aguzzi A., Pizzoferrato L. Nutritional value of mushrooms widely consumed in Italy. Food Chem. 2001, 73:321-325.
34. Mau J.L., Lin H.C., Chen C.C. Antioxidant properties of several medicinal mushrooms. J. Agric. Food Chem. 2002, 50:6072-6077.
35. Mikulski D., Zduńczyk Z., Jankowski J., Wiliczkiewicz A., Wertelecki T., Skorupinska J. Effects of organic acids or natural plant extracts added to diets for turkeys on growth performance, gastrointestinal tract metabolism and carcass characteristics. J. Anim. Feed Sci. 2008, 17:233-246.
36. Miles R.D., Butcher G.B., Henry P.R., Littell R.C. Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poult. Sci. 2006, 85:476-485.
37. Moriya J., Fachin L., Lourdes Neves Gândara A., Hanada Viotto W. Evaluation of culture media for counts of Bifidobacterium animalis in the presence of yoghurt bacteria. Braz. J. Microbiol. 2006, 37:516-520.
38. Mountzouris K.C., Tsirtsikos P., Kalamara E., Nitsch S., Schatzmayr G., Fegeros K. Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult. Sci. 2007, 86:309-317.
39. National Research Council Nutrient Requirements of Poultry 1994, Natl Acad. Press, Washington, DC. ninth rev. ed.
40. National Research Council Guide for the Care and Use of Laboratory Animals, Institute of Laboratory Animal resources, Commission on Life Sciences 1996, National Academy Press, Washington, DC.
41. Nisianakis P., Giannenas I., Gavriil A., Kontopidis G., Kyriazakis I. Variation in trace element contents among chicken, turkey, duck, goose, and pigeon eggs analyzed by inductively coupled plasma mass spectrometry (ICP-MS). Biol. Trace Elem. Res. 2009, 128:62-71.
42. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Chem. Med. 1967, 70:158-169.
43. Papageorgiou G., Botsoglou N.A., Govaris A., Giannenas I., Iliadis S., Botsoglou E. Iron-induced lipid oxidation of turkey liver, heart, breast and thigh tissues in response to dietary supplementation with oregano oil and alpha-tocopheryl acetate. Free Rad. Res. 2003, 37:67.
44. Rehman H., Böhm J., Zentek J. Effects of diets with insulin and sucrose on the microbial fermentation in the gastrointestinal tract of broilers. Proc. Soc. Nutr. Physiol. 2006, 15:155-158.
45. Rehman H., Rosenkranz C., Böhm J., Zentek J. Dietary inulin affects the morphology but not the sodium dependent glucose and glutamine transport in the jejunum of broilers. Poult. Sci. 2007, 86:118-122.
46. Rehman H., Vahjen W., Awad W.A., Zentek J. Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broilers. Arch. Anim. Nutr. 2007, 61:319-335.
47. Rolfe R.D. The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 2000, 130:396S-402S.
48. Rybka S., Kailasapathy K. Media for the enumeration of yoghurt bacteria. Int. Dairy J. 1996, 6:839-850.
49. Scardovi V. Irregular nonsporing Gram-positive rods: Genus Bifidobacterium. Bergey's Manual of Systematic Bacteriology 1986, vol. 2':1418-1434. Williams and Wilkins, Baltimore, Orla-Jensen.
50. Schneeman B.D. Pancreatic and digestive function. Dietary Fibre in Health and Disease 1982, 73-83. Plenum Press, New York. G.V. Vahuoung, D. Kritchevsky (Eds.).
51. Sims M.D., Dawson K.A., Newman K.E., Spring P., Hooge D.M. Effects of mannan oligosaccharide, bacitracin methylene disalicyclate, or both on live performance and intestinal microbiology of turkeys. Poult. Sci. 2004, 83:1148-1154.
52. Staal G.E., Visser J., Veeger C. Purification and properties of glutathione reductase of human erythrocytes. Biochim. Biophys. Acta 1969, 8:39-48.
53. Stanley V.G., Brown C., Sefton A.E. Comparative evaluation of a yeast culture, mannanoligosaccharide and an antibiotic on performance of turkeys. Poult. Sci. 2000, 79S:117.
54. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione Applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
55. Van der Wielen P.W., Lipman L.J., Van Knapen F., Biesterveld S. Competitive exclusion of Salmonella enterica serovar Enteritidis by Lactobacillus crispatus and Clostridium lactatifermentans in a sequencing fed-batch culture. Appl. Environ. Microbiol. 2002, 68:555-559.
56. Vetter J., Lelley J. Selenium level of the cultivated mushroom Agaricus bisporus. Acta Aliment. 2004, 33:297-301.
57. Vetter J. Chemical composition of eight edible mushrooms. Zeit. Lebens. Unters. Forschung 1993, 196:224-227.
58. Vetter J. Chemical composition of fresh and conserved Agaricus bisporus mushroom. Eur. Food Res. Technol. 2003, 217:10-12.
59. Willis W.L., Isikhuemhen O.S., Ibrahim S.A. Performance assessment of broiler chickens given mushroom extract alone or in combination with probiotics. Poult. Sci. 2007, 86:1856-1860.
60. Willis W.L., Murray C., Talbott C. Campylobacter isolation trends of cage versus floor broiler chickens: a one-year study. Poult. Sci. 2002, 81:629-631.
61. Yang J.H., Lin H.C., Mau J.L. Antioxidant properties of several commercial mushrooms. Food Chem. 2002, 77:229-235.
62. Yang W.M., Liu J.K., Hu L., Dong Z.J., Wu W.L., Chen Z.H. Antioxidant properties of natural p-terplenyl derivatives from the mushroom Thelephora ganbajun. J. Biosci. 2004, 59:359-362.
63. Yason C.V., Summers B.A., Schat K.A. Pathogenesis of rotavirus infection in various age groups of chickens and turkeys. Pathol. Am. J. Vet. Res. 1987, 48:927-938.