Intestinal events and nutritional dynamics predispose Clostridium perfringens virulence in broilers

Poultry Science

Volumn 93, Issue 12, 2014, Pages 3028-3036

  Moran, Edwin T ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Clostridium perfringens; Necrotic enteritis; Small intestine

Indexed keywords

ANIMAL; BIRD DISEASE; CHICKEN; CLOSTRIDIUM INFECTION; CLOSTRIDIUM PERFRINGENS; INTESTINE; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; VETERINARY; VIRULENCE;

ANIMALS; CHICKENS; CLOSTRIDIUM INFECTIONS; CLOSTRIDIUM PERFRINGENS; INTESTINES; POULTRY DISEASES; VIRULENCE;

EID: 84929035714     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2014-04313     Document Type: Review

References (104)

1. Aharinejad, S., A. Lametschwandtner, P. Franz, and W. Firbas. 1991. The vascularization of the digestive tract studied by scanning electron microscopy with special emphasis, on the teeth, esophagus, stomach, small and large intestine, pancreas, and liver. Scanning Microsc. 5:811-849.
2. Atuma, C., V. Strugala, A. Allan, and L. Holm. 2001. The adherent gastrointestinal mucus layer: Thickness and physical state in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G922-G929.
3. Baba, E., A. L. Fuller, J. M. Gilbert, S. G. Thayer, and L. R. McDougald. 1992. Effects of Eimeria brunetti infection and dietary zinc on experimental induction of necrotic enteritis in broiler chickens. Avian Dis. 36:59-62.
4. Baba, E., T. Ikemoto, T. Fukata, K. Sasai, A. Arakawa, and L. R. McDougal. 1997. Clostridial population and the intestinal lesions in chickens infected with Clostridium perfringens an Eimeria necatrix. Vet. Microbiol. 54:301-308.
5. Barrier-Guillot, B., z. C. Jondreville, A. M. Changneau, M. Larbier, and M. Leuillet. 1993. Effect of heat drying temperature on the nutritive value of corn in chickens and pigs. Anim. Feed Sci. Technol. 41:149-159.
6. Bayer, R. C., C. B. Chawan, F. H. Bird, and S. D. Musgrave. 1975. Characteristics of the absorptive surface of the small intestine of the chicken from 1 day to 14 weeks of age. Poult. Sci. 54:155-169.
7. Bird, F. H. 1971. Distribution of trypsin and α-amylase activities in the duodenum of the domestic bird. Br. Poult. Sci. 12:373-378.
8. Bohak, z. 1969. Purification and characterization of chicken pepsinogen and chicken pepsin. J. Biol. Chem. 244:4638-4648.
9. Branton, S. L., B. D. Lott, J. D. May, P. A. Hendin, F. W. Austin, M. A. Latour, and E. J. Day. 1996. The effects of nonautoclaved and autoclaved water-soluble wheat extracts on the growth of Clostridium perfringens. Poult. Sci. 75:335-338.
10. Chapman, H. D., P. L. Matsler, V. K. Muthavarapu, and M. E. Chapman. 2005. Acquisition of immunity to Eimeria maxima in newly hatched chickens given 100 oocysts. Avian Dis. 49:426-429.
11. Chawan, C. B., F. H. Bird, and R. W. Gerry. 1978. Relationship between intestinal movements and pancreatic juice secretion in the domestic chicken. Poult. Sci. 57:1084-1086.
12. Choi, J. H., G. B. Kim, and C. J. Cha. 2014. Spatial heterogeneity and stability of bacterial community in the gastrointestinal tracts of broiler chickens. Poult. Sci. 93:1942-1950.
13. Chow, W. L., and Y. K. Lee. 2008. Free fucose is a danger signal to human intestinal epithelial cells. Br. J. Nutr. 99:449-454.
14. Clench, M. H., P. M. Pineiro-Carrero, and J. R. Mathias. 1989. Migrating myoelectric complex demonstrated in four avian species. Am. J. Physiol. 256:G598-G603.
15. Collier, C. T., J. D. van der Klis, D. Deplanke, D. B. Anderson, and H. R. Gaskins. 2003. Effects of tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis. Antimicrob. Agents Chemother. 47:3311-3317.
16. Cowieson, A. J., T. Acamovic, and M. R. Bedford. 2006. Supplementation of corn-soy based diets with an Escherichia coli-derived phytase: Effects on broiler chick performance and the digestibility of amino acids and metabolizability of minerals and energy. Poult. Sci. 85:1389-1397.
17. Cowieson, A. J., and O. Adeola. 2005. Carbohydrases, protease, and phytase have an additive beneficial effect in nutritional marginal diets for broiler chicks. Poult. Sci. 84:1860-1867.
18. Cowieson, A. J., M. R. Bedford, P. H. Selle, and V. Ravindran. 2009. Phytate and microbial phytase: Implications for endogenous nitrogen losses and nutrient availability. World's Poult. Sci. Assoc. J. 65:401-417.
19. Craven, S. E. 2000. Colonization of the intestinal tract by Clostridium perfringens and fecal shedding in diet-distressed and unstressed broiler chickens. Poult. Sci. 79:843-849.
20. Craven, S. E., N. A. Cox, N. J. Stern, and J. M. Mauldin. 2001a. Prevalence of Clostridium perfringens commercial broiler hatcheries. Avian Dis. 45:1050-1053.
21. Craven, S. E., N. J. Stern, J. S. Bailey, and N. A. Cox. 2001b. Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Dis. 45:887-896.
22. Crea, F., P. Crea, A. De Robertis, and S. Sammartano. 2004. Speciation of phytate ion in aqueous solution. Characterization of Ca-phytate sparingly soluble species. Chem. Spec. Bioavail. 16:53-59.
23. Cressman, M. D., z. Yu, M. C. Nelson, S. J. Moeller, M. J. Lilburn, and H. N. zerby. 2010. Interrelations between the microbiotas in the litter and in the intestines of commercial broiler chickens. Appl. Environ. Microbiol. 76:6572-6582.
24. Dahiya, J. P., D. Hoehler, A. G. VanKessel, and M. D. Drew. 2007. Effect of different dietary methionine sources on intestinal microbial populations in broiler chickens. Poult. Sci. 86:2358-2366.
25. Dahiya, J. P., D. C. Wicked, A. G. Van Kassel, and M. D. Drew. 2006. Potential strategies for controlling necrotic enteritis in broiler chickens during the post-antibiotic era. Anim. Feed Sci. Technol. 129:60-88.
26. Daniel, H., B. Neugebauer, A. Kratz, and G. Rehner. 1985. Localization of acid microclimate along intestinal villi of rat jejunum. Am. J. Physiol. 248:G293-G298.
27. Deplancke, B., O. Vidal, D. Ganessunker, S. M. Donovan, R. I. Mackie, and H. R. Gaskins. 2002. Selective growth of mucolytic bacteria including Clostridium perfringens in a neonatal piglet model of total parental nutrition. Am. J. Clin. Nutr. 76:1117-1125.
28. Drew, M. D., N. A. Syed, B. G. Goldade, B. Laarveld, and A. G. VanKessel. 2004. Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens. Poult. Sci. 83:414-420.
29. Duke, G. E. 1982. Gastrointestinal motility and its regulation. Poult. Sci. 61:1245-1256.
30. Ferrer, R., J. M. Planas, and M. Moreto. 1995. Cell apical surface area in enterocytes from chicken, small and large intestine during development. Poult. Sci. 74:1995-2002.
31. Fisher, D. K., and D. B. Thompson. 1997. Retrogradation of maize starch after thermal treatment within and above the gelatinization temperature range. Cereal Chem. 74:344-351.
32. Flood, P. R. 1981. On the ultra structure of mucus. Biomed. Res. 2:49-53.
33. Fuchs, A. R., and G. J. Blonde. 1957. The nutritional requirements of Clostridia perfringens. J. Gen. Microbiol. 16:317-329.
34. Fuller, R., and D. J. Jayne-Williams. 1970. Resistance of the fowl (Gallus domesticus) to invasion by its intestinal flora II. Clearance of translocated intestinal bacteria. Res. Vet. Sci. 11:368-374.
35. Garcia, R. A., and J. G. Phillips. 2009. Physical distribution and characteristics of meat and bone meal protein. J. Sci. Food Agric. 89:329-336.
36. Granger, H. J., and R. A. Nyhof. 1982. Dynamics of intestinal oxygenation: Interactions between oxygen supply and uptake. Am. J. Physiol. 243:G91-G96.
37. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
38. Guo, S., D. Liu, X. zhao, C. Li, and Y. Guo. 2014. Xylanase supplementation of a wheat-based diet improved nutrient digestion and mRNA expression of intestinal nutrient transporters in broiler chickens infected with Clostridium perfringens. Poult. Sci. 93:94-103.
39. Hartemink, R., K. M. J. VanLaere, A. K. C. Mertens, and F. M. Rombouts. 1996. Fermentation of xyloglucan by intestinal bacteria. Anaerobe 2:223-230.
40. Hegedus, M., J. Bokori, and E. Andrasofszky. 1989. The value of crude protein content and in vitro pepsin digestibility of abattoir by-product meals in the prediction of their available protein content. Acta Vet. Hung. 37:27-33.
41. Hillman, K., A. L. Whyte, and C. S. Stewart. 1993. Dissolved oxygen in the porcine gastrointestinal tract. Lett. Appl. Microbiol. 16:299-302.
42. Holman, J. 1975. Fine structural changes of senescent enterocytes in the extrusion zone of chicken intestinal villi. Acta Vet. (Brno) 44:3-8.
43. Hubener, K., W. Vahjen, and O. Simon. 2002. Bacterial responses to different dietary cereal types and xylanase supplementation in the intestine of broiler chicken. Arch. Anim. Nutr. 56:167-187.
44. Humbert, W., J. C. Voegel, R. Kirsch, and V. Simonneeaux. 1989. Role of intestinal mucus in crystal biogenesis: An electron-microscopical, diffraction and x-ray micro analytical study. Cell Tissue Res. 255:575-583.
45. Jarmund, T., and W. Telle. 1982. Binding of Clostridium perfringens enterotoxin to hepatocytes, small intestinal epithelial cells and vero cells. Acta Pathol. Microbiol. Immunol. Scand. Sec. B 90:377-381.
46. Jia, W., B. A. Slominski, H. L. Bruce, G. Blank, G. Crow, and O. Jones. 2009. Effects of diet type and enzyme addition on growth performance and gut health of broiler chickens during subclinical Clostridium perfringens challenge. Poult. Sci. 88:132-140.
47. Kaldhusdal, M., O. Evensen, and T. Landsverk. 1995. Clostridium perfringens necrotizing enteritis of the fowl: A light microscopic, immunohistochemical and ultrastructural study of spontaneous disease. Avian Pathol. 24:421-433.
48. Kaldhusdal, M., C. Schneitz, M. Hofshagen, and E. Skjerve. 2001. Reduced incidence of Clostridium perfringens-associated lesions and improved performance in broiler chickens treated with normal intestinal bacteria from adult fowl. Avian Dis. 45:149-156.
49. Kaufman, H. W., and I. Kleinberg. 1971. The effect of pH on calcium binding by phytic acid and its inositol phosphoric acid derivatives and on the solubility of their calcium salts. Arch. Oral Biol. 16:445-460.
50. Keyburn, A. L., J. D. Boyce, P. Vaz, T. L. Bannam, M. E. Ford, and D. Parker. 2008. NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathog. 4:e26.
51. Keyburn, A. L., S. A. Sheedy, M. E. Ford, M. M. Williamson, M. M. Awad, J. I. Rood, and R. J. Moore. 2006. Alpha toxin of Clostridium perfringens is not an essential virulence factor in necrotic enteritis in chickens. Infect. Immun. 74:6496-6500.
52. Keyburn, A. L., X. X. Yan, T. L. Bannam, F. Van Emmerseel, J. I. Rood, and R. J. Moore. 2010. Association between avian necrotic enteritis and Clostridium perfringens strains expressing NetB toxin. Vet. Res. 41:21.
53. Khattak, F. M., T. Acamovic, and A. J. Cowieson. 2009. The response of chicks, with prior exposure to low and high phytate diets, when subsequently fed diets supplemented with phytase and phytate. Br. Poult. Abstr. 9:35-37.
54. Lensing, M., J. D. Van Der Klis, L. L. Bellego, and M. Rovers. 2007. The threonine requirement of broiler chickens encountering subclinical intestinal infection. Pages 343-346 in 16th European Symposium on Poultry Nutrition, Strasbourg, France.
55. Lovland, A., and M. Kaldhusdal. 1999. Liver lesions seen at slaughter as an indicator of necrotic enteritis in broiler flocks. FEMS Immunol. Med. Microbiol. 24:345-351.
56. Luciano, L., S. Groos, K. R. Rao, P. D. Gupta, and A. Reale. 1997. Early morphological events during apoptotic process in enterocytes. Pages 393-395 in Recent Advances Microscopy of Cells, Tissues and Organs. P. M. Motta, ed. Rome, Italy.
57. Macagno, E. O., J. Christensen, and C. L. Lee. 1982. Modeling the effect of wall movement on absorption in the intestine. Am. J. Physiol. 243:G541-G550.
58. Macfarlane, G. T., S. Hays, and G. R. Gibson. 1989. Influence of mucin on glycosidase, protease and arylamidase activities of human gut bacteria grown in a 3-stage continuous culture system. J. Appl. Bacteriol. 66:407-417.
59. Martin, T. G. 2010. The importance of the strain of C. perfringens in the development of necrotic enteritis. PhD Diss. University of Connecticut, Storrs.
60. Matheson, P. J., M. A. Wilson, and R. N. Garrison. 2000. Regulation of intestinal blood flow. J. Surg. Res. 93:182-196.
61. McDevitt, R. M., J. M. Brooker, T. Acamovic, and N. H. C. Sparks. 2006. Necrotic enteritis: A continuing challenge for the poultry industry. World's Poult. Sci. J. 62:221-224.
62. Mishima, T., M. Hisamatsu, W. S. York, K. Teranishi, and T. Yamada. 1998. Adhesion of β-D-glucans to cellulose. Carbohydr. Res. 308:389-395.
63. Moran, E. T. 1982. Comparative Nutrition of Fowl and Swine: The Gastrointestinal Systems. University of Guelph, Canada.
64. Moran, E. T. Jr. 1985. Digestion and absorption of carbohydrates in fowl and events through perinatal development. J. Nutr. 115:665-674.
65. Moran, E. T. 2010. Absorptive surface, mucin and phytin. Pages 64-66 in Proc. Int. Phytase Summit, Washington, DC.
66. Muhammed, S. I., S. M. Morrison, and W. I. Boyd. 1975. Nutritional requirements for nutrition and growth of Clostridium perfingens. J. Appl. Bacteriol. 38:248-253.
67. O'Brian, S., and Y.-J. T. Wang. 2007. Susceptibility of annealed starches to hydrolysis by α-amylase and glucoamylase. Carbohydr. Polym. 72:597-607.
68. Olkowski, A. A., C. Wojnarowicz, M. Chirino-Trejo, B. Laarveld, and G. Sawicki. 2008. Sub-clinical necrotic enteritis in broiler chickens: Novel etiological consideration based on ultra-structural and molecular changes in the intestinal tissue. Res. Vet. Sci. 85:543-553.
69. Onyango, E. M., E. K. Asem, and O. Adeola. 2009. Phytic acid increases mucin and endogenous amino acid losses from the gastrointestinal tract of chickens. Br. J. Nutr. 101:836-842.
70. Palliyeguru, M. W. C. D., S. P. Rose, and A. M. Mackenzie. 2010. Effect of dietary protein concentrates on the incidence of subclinical necrotic enteritis and growth performance of broiler chickens. Poult. Sci. 89:34-43.
71. Park, S.-W., G. zhen, C. Verhaeghe, Y. Nakagami, L. T. Nguyenvu, A. J. Barczak, N. Kiilleen, and D. J. Erie. 2009. The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc. Natl. Acad. Sci. USA 106:6950-6955.
72. Parsons, C. M., F. Castanon, and Y. Han. 1997. Protein and amino acid quality of meat and bone meal. Poult. Sci. 76:361-368.
73. Paz, H. B., A. S. Tisdale, Y. Danjo, S. J. Spurr-Michaud, P. Argueso, and I. K. Gipson. 2003. The role of calcium in mucin packaging within goblet cells. Exp. Eye Res. 77:69-75.
74. Pedersen, K., L. Bjerrum, O. E. Heuer, D. M. A. Lo Fo Wong, and B. Nauerby. 2008. Reproducible infection model for Clostridium perfringens in broiler chickens. Avian Dis. 52:34-39.
75. Perez-Vilar, J. 2007. Mucin granule intraluminar organization. Am. J. Respir. Cell Mol. Biol. 36:183-190.
76. Petit, L., M. Gilbert, and M. R. Popoff. 1999. Clostridium perfringens toxinotypes and genotype. Trends Microbiol. 7:104-110.
77. Pirgozliev, V., M. R. Bedford, T. Acamovic, and M. Allimehr. 2011. The effects of supplementary bacterial phytase on dietary true metabolizable energy, nutrient digestibility and endogenous losses in precision fed turkeys. Br. Poult. Sci. 52:214-220.
78. Potten, C. S., and T. D. Allen. 1977. Ultrastructure of cell loss in intestinal mucosa. J. Ultrastruct. Res. 60:272-277.
79. Ravindran, V. 2013. Feed enzymes: Science, practice and metabolic realities. J. Appl. Poult. Sci. 22:628-636.
80. Ravindran, V., W. H. Hendriks, B. J. Camden, D. V. Thomas, P. C. H. Morel, and C. A. Butts. 2002. Amino acid digestibility of meat and bone meals for broiler chicken. Aust. J. Agric. Res. 53:1257-1264.
81. Rehman, H. U., W. Vahjien, W. A. Awad, and J. zentek. 2007. Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch. Anim. Nutr. 61:319-335.
82. Rhodes, D. I., and B. A. Stone. 2002. Proteins in cells of wheat aleurone cells. J. Cereal Sci. 36:83-101.
83. Robertson, J. A., G. Majsak-Newmwn, and S. G. Ring. 1997. Release of mixed linkage (1→3), (1→4) β-D-glucans from barley by protease activity and effects on ileal effluent. Int. J. Biol. Macromol. 21:57-60.
84. Sasaki, J., M. Goryo, M. Makara, K. Nakamura, and K. Okada. 2003. Necrotic hepatitis due to Clostridium perfringens infection in newly hatched broiler chicks. J. Vet. Med. Sci. 65:1249-1251.
85. Shehata, A. T., J. Lerner, and D. S. Miller. 1984. Development of nutrient transport systems in chick jejunum. Am. J. Physiol. 246:G101-G107.
86. Shepherd, A. P., and J. W. Kiel. 1992. A model of countercurrent shunting of oxygen in the intestinal villus. Am. J. Physiol. (Heart Circ. Physiol.) 262:H1136-H1142.
87. Shiau, Y.-F., P. Fernandez, M. J. Jackson, and S. McMonagle. 1985. Mechanisms maintaining a low-pH microclimate in the intestine. Am. J. Physiol. 248:G608-G617.
88. Shojadoost, B., A. R. Vince, and J. F. Prescott. 2012. The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: A critical review. Vet. Res. 43:74-86.
89. Smedley, J. G. III, D. J. Fisher, S. Sayeed, G. Chakrabaru, and B. A. McClane. 2004. The enteric toxins of Clostridium perfringens. Rev. Physiol. Biochem. Pharmacol. 152:183-204.
90. Star, L., M. Rovers, E. Corrent, and J. D. Van der Klis. 2012. Threonine requirement of broiler chickens during subclinical intestinal Clostridium infection. Poult. Sci. 91:643-652.
91. Tankson, J. D., J. P. Thaxton, and Y. Vizzier-Thaxton. 2002. Bacteria in heart and lungs of young chicks. J. Appl. Microbiol. 92:443-450.
92. Teshfam, M., and S. Rahbari. 2003. Alteration in small intestinal structure induced by experimental subclinical coccidiosis in chicken. J. Appl. Anim. Res. 24:33-39.
93. Timbermont, L., F. Haesebrouck, R. Ducatelle, and F. Van Immerseel. 2011. Necrotic enteritis in broilers an updated review on the pathogenesis. Avian Pathol. 40:341-347.
94. Timbermont, L., A. Lanckriet, F. Pasmans, F. Haesebrouck, R. Ducatelle, and F. Van Immerseel. 2009. Intra-species growthinhibition by Clostridium perfringens is a possible virulence trait in necrotic enteritis in broilers. Vet. Microbiol. 137:388-391.
95. Turk, D. E. 1982. The anatomy of the avian digestive tract as related to feed utilization. Poult. Sci. 61:1225-1244.
96. Uzal, F. A., J. C. Freedman, A. Shrestha, J. R. Theoret, J. Garcia, M. M. Awad, V. Adams, R. J. Moore, J. I. Rood, and B. A. McClane. 2014. Towards an understanding of the role of Clostridium perfringens toxins in human animal disease. Future Microbiol. 9:361-377.
97. Van Immerseel, F., J. I. Rood, R. J. Moore, and R. W. Titball. 2009. Rethinking our understanding of the pathogenesis of necrotic enteritis in broilers. Trends Microbiol. 17:32-36.
98. Vissiennon, T., S. Menger, and I. Langhof. 1996. Hepatic and renal ultrastructural lesions in experimental Clostridium perfringens type A enterotoxemia in chickens. Avian Dis. 40:720-724.
99. Voeten, F. O., and M. Van Rijen. 1987. An analysis of the losses from subclinical coccidiosis of the small intestine caused by Eimeria acervulina and Eimeria maxima under field conditions. Personal Communication Publication. Animal Health Services in Noord-Brabant, Molenwijkseweg, Boxtel, the Netherlands.
100. Walk, C. L., M. R. Bedford, T. S. Santos, D. Pavia, J. R. Bradley, H. Wladecki, C. Honaker, and A. P. McElroy. 2013. Extra-phosphoric effects of superdoses of a novel microbial phytase. Poult. Sci. 92:719-725.
101. Wilkie, D. C., A. G. Van Kassel, L. J. White, B. Laarveld, and M. D. Drew. 2005. Dietary amino acids affect intestinal Clostridium perfringens populations in broiler chickens. Can. J. Anim. Sci. 85:185-193.
102. Williams, z. T., and K. S. Macklin. 2013. Stratification of bacterial concentrations, from upper to lower, in broiler litter. J. Appl. Poult. Sci. 22:492-498.
103. Wold, J. K., T. Midtvedt, and R. W. Jeanloz. 1974. Intestinal glycoproteins of germfree rats. III. Characterization of a water-soluble glycoprotein fraction. Acta Chem. Scand. B 28:277-284.
104. Yamauchi, K.-E., and Y. Isshiki. 1991. Scanning electron microscopic observations on the intestinal villi in growing white leghorn and broiler chickens from 1 to 30 days of age. Br. J. Poult. Sci. 32:67-78.