Hostname: page-component-7dd5485656-6kn8j Total loading time: 0 Render date: 2025-10-31T12:09:12.139Z Has data issue: false hasContentIssue false
  • English
  • Français

Necrotic enteritis; a continuing challenge for the poultry industry

Published online by Cambridge University Press:  18 September 2007

R.M. McDevitt ,
J.D. Brooker ,
T. Acamovic  and
N.H.C. Sparks
R.M. McDevitt*
Affiliation:
Avian Science Research Centre, Animal Health Group, SAC Edinburgh, West Mains Road, Edinburgh EH9 3JG, United Kingdom
J.D. Brooker
Affiliation:
Avian Science Research Centre, Animal Health Group, SAC Edinburgh, West Mains Road, Edinburgh EH9 3JG, United Kingdom
T. Acamovic
Affiliation:
Avian Science Research Centre, Animal Health Group, SAC Edinburgh, West Mains Road, Edinburgh EH9 3JG, United Kingdom
N.H.C. Sparks
Affiliation:
Avian Science Research Centre, Animal Health Group, SAC Edinburgh, West Mains Road, Edinburgh EH9 3JG, United Kingdom
*
*Corresponding author: regina.mcdevitt@sac.ac.uk
Get access

Abstract

Necrotic enteritis is a disease in poultry that can have a high economic and animal welfare cost, and has become increasingly prevalent in the European Union due to factors such as the removal of antibiotic growth promoters and the requirement to exclude animal by-products from diet formulations. Estimates of the prevalence of necrotic enteritis vary widely (1–40%) as does the cost of the disease, and the subclinical form may be the most important manifestation of the disease as this is likely to go undetected and hence untreated. An outbreak of necrotic enteritis is primarily associated with rapid proliferation of the anaerobic bacterium, Clostridium perfringens type A or C, leading to gaseous extension of the small intestine, the production of one or more exotoxins, and enteric toxicosis. The molecular progression of the disease is quite complex and at the bacterial level involves quorum sensing, toxin production and secretion, and interactions of the pathogen with the innate immune system of the chicken. Intestinal cell permeation by the toxin activates a series of intracellular pathways including protein kinase cascades, and ultimately results in cell death. The precise molecular signals that set off this cascade are still unclear. The various predisposing environmental, health and dietary factors that modify the gut environment and promote colonisation with C. perfringens, are discussed. With such a multi-factorial disease, a working and reproducible experimental model with which to study bacterial/host and dietary/host interactions is an essential tool in the search for appropriate control or management strategies for the poultry industry.

Keywords

necrotic enteritisClostridium perfringenschickensincidenceα-toxingene expressionexperimental model

Information

Type
Reviews
Information
World's Poultry Science Journal , Volume 62 , Issue 2 , June 2006 , pp. 221 - 247
Copyright
Copyright © Cambridge University Press 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Acamovic, T. (2001) Commercial application of enzyme technology for poultry production. World's Poultry Science Journal 57: 225–242.CrossRefGoogle Scholar
Acamovic, T., Stewart, C.S. and Pennycott, T.W. (2004) (Eds) Poisonous plants and related toxins. CAB International Wallingford. UK. Pp. 586.CrossRefGoogle Scholar
Allen, P.C., Danforth, H.D. and Levander, O.A. (1996) Diets high in n-3 fatty acids reduce cecal lesion scores in chickens infected with Eimeria tenella. Poultry Science 75: 179–185.CrossRefGoogle ScholarPubMed
Allen, P.C.Lydon, J. and Danforth, H.D. (1997) Effects of components of Artemisia annua on coccidia infections in chickens. Poultry Science 76: 1156–1163.Google Scholar
Al-Shiekhy, F. and Al-Saieg, A. (1980) Role of coccidia in the occurrence of necrotic enteritis of chickens. Avian Diseases 24: 324–333.CrossRefGoogle Scholar
Al-Shiekhy, F. and Truscott, R.B. (1977) The pathology of necrotic enteritis of chickens following infusion of crude toxins of Clostridium perfringens into the duodenum. Avian Diseases 21: 241–255.Google Scholar
Annett, C.B., Viste, J.R., Chirino-Trejo, M., Classen, H.L., Middleton, D.M. and Simko, E. (2002) Necrotic enteritis: effects of barley, wheat and corn diets on proliferation of Clostridium perfringens type A. Avian Pathology 31: 599–602.CrossRefGoogle ScholarPubMed
Apajalahti, J., Kettunen, A. and Graham, H. (2004) Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. World's Poultry Science Journal 60: 223–232.Google Scholar
Apajalahti, J., Sarkilahti, L.K., Maki, R.R., Heikkinen, J.P., Nurminen, P.H. and Holben, R. (1998) Effective recovery of bacterial DNAand percent-guanine-plus-cytosine-based analyses of community structure in the gastrointestinal tract of broiler chickens. Applied Environmental Microbiology 64: 4084–4088.Google Scholar
Asaoka, Y., Yannai, T., Hirayama, H., Une, Y., Saito, E., Sakai, H., Goryo, M., Fukushi, H. and Masegi, T. (2004) Fatal necrotic enteritis associated with Clostridium perfringens in wild crows (Corvus macrorhynchos). Avian Pathology 33: 19–24.Google Scholar
Baba, E., Fuller, A.L., Gilbert, J.M., Thayer, S.G. and Mcdougald, L.R. (1992) Effects of Eimeria-brunetti infection and dietary zinc on experimental induction of necrotic enteritis in broiler chickens. Avian Diseases 36: 59–62.Google Scholar
Bach Knudsen, K.E. (1997) Carbohydrate and lignin contents of plant materials used in animal feeding. Animal Feed Science and Technology 67: 319–338.Google Scholar
Bach Knudsen, K.E. and Jorgensen, H. (2000) Intestinal degradation of dietary carbohydrates – from birth to maturity. Digestive physiology in pigs. In: Proceedings of the 8th SymposiumSwedish University of Agricultural SciencesUppsala, Sweden Pp.109–120.Google Scholar
Bains, B.S. (2002) Anticoccidial prophylaxis and disease interactions. World Poultry 18(9): 57–59.Google Scholar
Barbosa, T.M., Serra, C.R., La Ragione, R.M., Woodward, M.J. and Henriques, A.O. (2005) Screening for Bacillus isolates in the broiler gastrointestinal tract. Applied and Environmental Microbiology 71: 968–978.CrossRefGoogle ScholarPubMed
Barnes, E.M., Mead, G.C., Barnum, D.A. and Harrye, G. (1972) The intestinal flora of the chicken in the period 2 to 6 weeks of age, with particular reference to the anaerobic bacteria. British Poultry Science 13 : 311–326.CrossRefGoogle Scholar
Bedford, M. (2000) Removal of antibiotic growth promotors from poultry diets: implications and strategies to minimise subsequent problems. World's Poultry Science Journal 56: 347–365.CrossRefGoogle Scholar
Bedford, M.R. and Apajalahti, J. (2000) Microbial interactions in the response to exogenous enzyme utilization. In: Enzymes in farm animal nutrition. Bedford, M.R (ed) Pp. 299–314.Google Scholar
Bento, M.H.L., Acamovic, T. and Makkar, H.P.S. (2005) The influence of tannin, pectin and polyethylene glycol on attachment of 15N-labelled rumen microorganisms to cellulose. Animal Feed Science and Technology In press.CrossRefGoogle Scholar
Bento, M.H.L., Acamovic, T. and Makkar, H.P.S. (2005b) Effect of mimosa tannin and pectin on microbial protein synthesis and gas production during in vitro fermentation of 15N-labelled maize shoots. Animal Feed Science and Technology In press.Google Scholar
Berkhoff, H.A. (1985) Clostridium colinum sp. nov, the causative agent of ulcerative enteritis (quail disease) in quail, chickens, and pheasants. International Journal of Systematic Bacteriology 35: 155–159.Google Scholar
Bildfell, R.J., Eltzroth, E.K. and Songer, J.G. (2001) Enteritis as a cause of mortality in the Western Bluebird (Sialia mexicana). Avian Diseases 45: 760–763.CrossRefGoogle ScholarPubMed
Boulliane, M. (1999) Can we farm poultry without antimicrobials? Publication of the Ontario Ministry of Agriculture, Food and Rural Affairs. Queen's Printer for Ontario, Ontario Canada. http://www.gov.on.ca/OMAFRA/english/livestock/animalcare/amr/facts/boulianne.htmGoogle Scholar
Branton, S.L., Lott, B.D., May, J.D., Hedin, P.A., Austin, F.W., Latour, M.A. and Day, E.J. (1997) The effects of nonautoclaved and autoclaved water-soluble wheat extracts on the growth of Clostridium perfringens. Poultry Science 75: 335–338.Google Scholar
Broussard, C.T., Hofacre, C.L., Page, R.K. and Fletcher, O.J. (1986) Necrotic enteritis in cage-reared commercial layer pullets. Avian Disease 30: 617–619.CrossRefGoogle ScholarPubMed
Bueschel, D.M., Jost, B.H., Billington, S.J., Trinh, H.T. and Songer, J.G. (2003) Prevalence of cpb2, encoding beta2 toxin, in Clostridium perfringens field isolates: correlation of genotype with phenotype. Veterinary Microbiology 94: 121–129.CrossRefGoogle ScholarPubMed
Calderon, A.M., Buck, G. and Doyle, R.J. (1997) Lectin-microorganism complexes. In: Lectins, Biology, Biochemistry, Clinical Biochemistry, Volume 12, Van Driessche, E.Beeckmans, S. and Bøg-Hansen, T.C. (Eds) Textop, Hellerup Denmark.Google Scholar
Carre, B. (2004) Causes for variation in digestibility of starch among feedstuffs. World's Poultry Science Journal 60: 76–89.CrossRefGoogle Scholar
Casewell, M., Friis, C., Granell, E.M., Mcmullin, P. and Phillips, I. (2003) The European ban on growth-promoting antibiotics and its consequences for human and animal health. Journal of Antimicrobial Chemotherapy 52: 159–161.CrossRefGoogle ScholarPubMed
Clarke, E. and Wiseman, J. (2005) Effects of variable trypsin inhibitor content of soyabean meal on true and apparent ileal digestibility of amino acids and pancreas size in broiler chickens. Animal Feed Science and technology 121: 125–138.Google Scholar
Clarke, E. and Wiseman, J. (2004) Effect of varying trypsin inhibitor activity of full fat soya on nutritional value for broiler chicks. In: Poisonous plants and related toxins. Acamovic, T., Stewart, C.S. and Pennycott, T.W. (Eds) CAB International, Wallingford. UK Pp. 512–519.CrossRefGoogle Scholar
Chesson, A. (2001) Non-starch degrading enzymes in poultry diets: influence of ingredients on the selection of activities. World's Poultry Science Journal 57: 251–263.Google Scholar
Choct, M. (2001) Enzyme supplementation of poultry diets based on viscous cereals. In: Enzymes in Farm Animal Nutrition (Bedford, M.R. and Partridge, GG Eds), CABI, Wallingford UK. Pp 145–160.Google Scholar
Choct, M., Hughes, R.J., Wang, J., Bedford, M.R., Morgan, A.J. and Annison, G. (1996) Increased small intestinal fermentation is partly responsible for the anti-nutritive activity of non-starch polysaccharides in chickens. British Poultry Science 37: 609–621.CrossRefGoogle ScholarPubMed
Cowen, B.S., Schwartz, L.D., Wilson, R.A. and Ambrus, S.I. (1987) Experimentally induced necrotic enteritis in chickens. Avian Diseases 31: 904–906.Google Scholar
Craven, S.E., Cox, N.A., Stern, N.J. and Mauldin, J.M. (2001a) Prevalence of Clostridium perfringens in commercial broiler hatcheries. Avian Diseases 45: 1050–1053.Google Scholar
Craven, S.E., Stern, N.J., Bailey, J.S. and Cox, N.A. (2001b) Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Diseases 45: 887–896.Google Scholar
Craven, S.E., Stern, N.J., Cox, N.A., Bailey, J.S. and Berrang, M. (1999) Cecal carriage of Clostridium perfringens in broiler chickens given Mucosal Starter Culture (TM). Avian Diseases 43: 484–490.Google Scholar
Cowieson, A.J. (2005) Factors that affect the nutritional value of maize for broilers. Animal Feed Science and Technology 119: 293–305.Google Scholar
Dibner, J.J. and Buttin, P. (2002) Use of organic acids as a model to study the impact of gut microflora on nutrition and metabolism. Journal of Applied Poultry Research 11: 453–463.CrossRefGoogle Scholar
D'mello, J.P.F. (1997) Handbook of Plant and Fungal Toxicants. CRC Press, Boca Raton, New York.Google Scholar
Danicke, S. (2002) Prevention and control of mycotoxins in the poultry production chain: a European perspective. World's Poultry Science Journal 58: 451–467.CrossRefGoogle Scholar
Danicke, S., Matthes, S., Halle, I., Ueberschar, K.H., Doll, S. and Valenta, H. (2003) Effects of graded levels of Fusarium toxin-contaminated wheat and of a detoxifying agent in broiler diets on performance, nutrient digestibility and blood chemical parameters. British Poultry Science 44: 113–126.Google Scholar
Donelli, G., Fiorentini, C., Matarrese, P., Falzano, L., Cardines, R., Mastrantonio, P., Payne, D. W. and Titball, R.W. (2003) Evidence for cytoskeletal changes secondary to plasma membrane functional alterations in the in vitro cell response to Clostridium perfringens epsilon-toxin. Comparative Immunology, Microbiology and Infectious Diseases 26: 145–156.Google Scholar
Droual, R., Farver, T.B. and Bickford, A.A. (1995) Relationship of sex, age, and concurrent intestinal disease to necrotic enteritis in turkeys. Avian Diseases 39: 599–605.CrossRefGoogle ScholarPubMed
Droual, R., Shivaprasad, H.L. and Chin, R.P. (1994) Coccidiosis and necrotic enteritis in turkeys. Avian Diseases 38: 177–183.Google Scholar
Elwinger, K., Berndston, E., Engstrom, B., Fossum, O. and Waldenstedt, L. (1998) Effect of antibiotic growth promotors and anticoccidials on growth of Clostridium perfringens in the caeca and on the performance of broiler chickens. Acta Veterinaria Scandinavica 39: 433–441.Google Scholar
Elwinger, K., Engstrom, B., Berndston, E., Fossum, O. and Teglof, B. (1992) The effects of narasin on Clostridium perfringens in caeca and the occurrence of necrotic enteritis in broiler chickens. In: Proceedings of XIX World's Poultry CongressAmsterdam, The Netherlands. Pp. 580–584.Google Scholar
Elwinger, K. and Teglof, B. (1991) Performance of broiler chickens as influenced by a dietary enzyme complex with and without antibiotic supplementation. Archives für Geflügelkunde 55: 69–73.Google Scholar
Emborg, H., Ersboll, A., Heuer, O. and Wegener, H.C. (2001) The effect of discontinuing the use of antimicrobial growth promotors on the productivity in the Danish broiler production. Preventative Veterinary Medicine 50: 53–70.CrossRefGoogle Scholar
Evans, M.C. and Wegener, H.C. (2003) Antimicrobial growth promotors and Salmonella spp., Campylobacter spp. in poultry and swine Denmark. Emerging Infectious Diseases 9: 489–492.Google Scholar
Fink-Gremmels, J. (2005) Mycotoxicosis in Animal Health. In: European Mycotoxin Seminar Series, Publication of Alltech Incorporated, Nicholasville USA. Pp.19–41.Google Scholar
Frame, D.D. and Bickford, A.A. (1986) An outbreak of coccidiosis and necrotic enteritis in 16-week-old cage-reared layer replacement pullets. Avian Diseases 30: 601–602.CrossRefGoogle ScholarPubMed
Garrido, M.N., Skjervheim, M., Oppegaard, H. and Sorum, H. (2004) Acidified litter benefits the intestinal flora balance of broiler chickens. Applied And Environmental Microbiology 70: 5208–5213.CrossRefGoogle ScholarPubMed
Gazdzinski, P. and Julian, R.J. (1992) Necrotic enteritis in turkeys. Avian Diseases 36: 792–798.CrossRefGoogle ScholarPubMed
Giannenas, I., Florou-Paneri, P., Papazahariadou, M., Christaki, E., Botsoglou, N.A. and Spais, A.B. (2003) Effect of dietary supplementation with oregano essential oil on performance of broilers after experimental infection with Eimeria tenella. Archives of Animal Nutrition 57: 99–106.CrossRefGoogle ScholarPubMed
Gilbert, C. and Slavik, M. (2004) Determination of toxicity of Campylobacter jejuni isolated from humans and from poultry carcasses acquired at various stages of production. Journal of Applied Microbiology 97: 347–353.Google Scholar
Gornowicz, E. (2004) Microbiological evaluation of poultry house environments as influenced by acidifying preparations added to compound feed. Medycyna Weterynaryjna 60: 755–758.Google Scholar
Grave, K., Kaldhusdal, M., Kruse, H., Fevang, R., Harr, L.M. and Flatlandsmo, K. (2004) What has happened in Norway after the ban of Avoparcin? Consumption of antimicrobials by poultry. Preventative Veterinary Medicine 62: 59–72Google Scholar
Helmbolt, C.F. and Bryant, E.S. (1971) The pathology of necrotic enteritis in domestic fowl. Avian Diseases 15: 775–780.Google Scholar
Hetland, H., Choct, M. and Svihus, B. (2004) Role of insoluble non-starch polysaccharides in poultry nutrition. World's Poultry Science Journal 60: 415–422.CrossRefGoogle Scholar
Haralampu, S.G. (2000) Resistant starch – a review of the physical properties and biological impact of RS3. Carbohydrate Polymers 41: 285–292.Google Scholar
Havard, H.L., Hunter, S.E.C. and Titball, R.W. (1992) Comparison of the nucleotide sequence and development of a PCR test for the epsilon toxin gene of Clostridium perfringens type B and type D. FEMS Microbiology Letters 97: 77–81.Google Scholar
Heier, B.T., Lovland, A., Soleim, K.B., Kaldhusdal, M. and Jarp, J. (2001) A field study of naturally occurring specific antibodies against Clostridium perfringens alpha toxin in Norwegian broiler flocks. Avian Diseases 45: 724–732.Google Scholar
Hermans, P.G. and Morgan, K.L. (2003) The epidemiology of necrotic enteritis in broiler chickens in the UK; a cross-sectional survey. In: 10th Symposium of the international Society of Veterinary Epidemiology and EconomicsChile17th –21st November.Google Scholar
Hetch, D.W., Vedantam, G. and Osmolski, J.R. (1999) Antimicrobial susceptibility testing, therapy (faculty presentation). Anaerobe 5: 421–429.Google Scholar
Hofacre, C.L., Johnson, A.C., Kelly, B.J. and Froyman, R. (2002) Effect of a commercial competitive exclusion culture on the reduction of colonization of an antibiotic-resistant pathogenic Escherichia coli in day-old broiler chickens. Avian Diseases 46: 198–202.Google Scholar
Hofacre, C.L., Froyman, R., Gautrias, B., George, B., Goodwin, M.A. and Brown, J. (1998) Use of aviguard and other intestinal bioproducts in experimental Clostridium perfringens-associated necrotizing enteritis in broiler chickens. Avian Diseases 42: 579–584Google Scholar
Hofshagen, M. and Kaldhusdal, M. (1992) Barley inclusion and avoparcin inclusion in broiler diets. 1. Effect on small intestinal bacterial flora and performance Poultry Science 71: 959–969.CrossRefGoogle ScholarPubMed
Hopwood, D.E., Pethick, D.W., Pluske, J.R. and Hampson, D.J. (2004) Addition of pearl barley to a rice-based diet for newly weaned piglets increases the viscosity of the intestinal contents, reduces starch digestibility and exacerbates post-weaning colibacillosis. British Journal of Nutrition 92: 419–427.Google Scholar
Van Immerseel, F., De Buck, J., Pasmans, F.Huyghebaert, G., Haesebrouck, F. and Ducatelle, R. (2004) Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathology 33: 537–549.Google Scholar
Van Immerseel, F., Cauwerts, K., Devriese, L.A., Haesebrouck, F. and Ducatelle, R. (2002) Feed additives to control Salmonella in poultry. Worlds Poultry Science Journal 58: 501–513.Google Scholar
Iji, P.A. and Tivey, D.R. (1998) Natural and synthetic oligosaccharides in broiler chicken diets. World's Poultry Science Journal 54: 129–143.Google Scholar
Impey, C.S., Mead, G.C. and George, S.M. (1982) Competitive exclusion of salmonellas from the chick caecum using a defined mixture of bacterial isolates from the caecal microflora of an adult bird. Journal of Hygiene 89: 479–490.Google Scholar
Inborr, J. (2001) Swedish poultry production without in-feed antibiotics – an opportunity for Clostridia? British Poultry Science 42: S64–S65.Google Scholar
Jackson, M.E.Anderson, D.M., Hsiao, H.Y., Mathis, G.F. and Fodge, D.W. (2003) Beneficial effect of beta -mannanase feed enzyme on performance of chicks challenged with Eimeria sp. and Clostridium perfringens. Avian Diseases 47: 759–763.Google Scholar
Joint Expertadvisorycommittee On Antibiotic Resistance (JETACAR) (1999) The use of antibiotics in food producing animals: antibiotic-resistant bacteria in animals and humans. Commonwealth of Australia. ISBN 1 86496 0612.Google Scholar
Juskiewicz, J., Zdunczyck, Z. and Jankowski, J. (2004) Selected parameters of gastrointestinal tract metabolism of turkeys fed diets with flavomycin and different inulin content. World's Poultry Science Journal 60: 177–185.Google Scholar
Justin, N., Walker, N., Bullifent, H.L., Songer, G., Bueschel, D.M., Jost, H., Naylor, C., Miller, J., Moss, D.S., Titball, R.W. and Basak, A.K. (2002) The first strain of Clostridium perfringens isolated from an azvian source has an alpha-toxin with divergent structural and kinetic properties. Biochemistry 41: 6253–6262.Google Scholar
Kaldhusdal, M. and Lovland, H. (2000) The economical impact of Clostridium perfringens is greater than anticipated. World Poultry 16: 50–51.Google Scholar
Kaldhusdal, M. and Skjerve, E. (1996) Association between cereal contents in the diet and incidence of necrotic enteritis in broiler chickens in Norway. Preventative Veterinary Medicine 28: 1–16.Google Scholar
Kaldhusdal, M. and Hofshagen, M. (1992) Barley inclusion and avoparcin inclusion in broiler diets. 2. Clinical, pathological and bacteriological findings in a mild form of necrotic enteritis. Poultry Science 71: 1145–1153.Google Scholar
Kaldhusdal, M., Schneitz, C., Hofshagen, M. and Skjerv, E. (2001) Reduced incidence of Clostridium perfringens-associated lesions and improved performance in broiler chickens treated with normal intestinal bacteria from adult fowl. Avian Diseases 45: 149–156.Google Scholar
Kaldhusdal, M., Hofshagen, A., Lovland, H., Langstrand, and Redhead, K. (2000) Necrotic enteritis challenge models with broiler chickens raised on litter: evaluation of preconditions, Clostridium perfringens strains and outcome variables. FEMS Immunology and Medical Microbiology 24: 337–343.Google Scholar
Kita, K., Nagao, K. and Okumura, J. (2005) Nutritional and tissue specificity of IGF-I and IGFBP-2 gene expression in growing chickens - A review. Asian-Australasian Journal of Animal Sciences 18: 747–754.Google Scholar
Klasing, K.C. (1998) Nutritional modulation of resistance to infectious diseases. Poultry Science 77: 1119–1125.Google Scholar
Kleessen, B., Hartmann, L. and Blaut, M. (2003) Fructans in the diet cause alterations of intestinal mucosal architecture, released mucins and mucosa-associated bifidobacteria in gnotobiotic rats. British Journal of Nutrition 89: 597–606.Google Scholar
Knarreborg, A., Simon, M.A., Engberg, R.M., Jensen, B.B., Tannock, G.W. (2002) Effects of dietary fat source and subtherapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens at various ages. Applied and Environmental Microbiology 68: 5918–5924.Google Scholar
Kocher, A., Choct, M., Ross, G., Broz, J. and Chung, T.K. (2003) Effects of enzyme combinations on apparent metabolizable energy of corn-soybean meal-based diets in broilers. Journal of Applied Poultry Research 12: 275–283.CrossRefGoogle Scholar
Lan, Y., Verstegen, M.W.A., Tamminga, S. and Williams, B.A. (2005) The role of the commensal gut microbial community in broiler chickens. World's Poultry Science Journal 61: 95–104.CrossRefGoogle Scholar
Langhout, D.J., Schutte, J.B., De Jong, J., Sloetjes, H., Verstegen, M.W.A. and Tamminga, S. (2000) Effect of viscosity on digestion of nutrients in conventional and germ-free chicks. British Journal of Nutrition 83: 533–540.CrossRefGoogle ScholarPubMed
La Ragione, R.M., Narbad, A., Gasson, M.J. and Woodward, M.J. (2004) In vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry. Letters in Applied Microbiology 38: 197–205.Google Scholar
Loveland, A. and Kaldhusdal, M. (2001) Severely impaired production performance in broiler flocks with high incidence of Clostridium perfringens associated hepatitis. Avian Pathology 30: 73–81.Google Scholar
Lovland, A., Kaldhusdal, M., Redhead, K., Skjerve, E. and Lillehaug, A. (2004) Maternal vaccination against subclinical necrotic enteritis in broilers. Avian Pathology 33: 83–92.Google Scholar
Lu, L.G., Hume, M.E. and Pillai, S.D. (2005) Autoinducer 2-like activity in poultry-associated enteric bacteria in response to subtherapeutic antibiotic exposure. Avian Diseases 49: 74–80.Google Scholar
Mansoori, B. and Acamovic, T. (1998a) The excretion of minerals from broilers fed tannic acid, polyethylene glycol and protein. In: Toxic Plants and Other Natural Toxicants. Garland, T. and Barr, A.C. (Eds) CAB International, London UK. Pp. 101–105.Google Scholar
Mansoori, B. and Acamovic, T. (1998b) The influence of tannic acid on amino acid digestibility by broilers. In: Toxic Plants and Other Natural Toxicants. Garland, T. and Barr, A.C. (Eds) CAB International, London UK. Pp. 106–110.Google Scholar
Martel, A., Devriese, L.A., Cauwerts, K., De Gaussem, K., Decostere, A. and Haesebrouck, F. (2004) Susceptibility of Clostridium perfringens strains from broiler chickens to antibiotics and anticoccidials. Avian Pathology 33: 3–7.Google Scholar
Mateos, G.G., Lazaro, R. and Gracia, M.I. (2002) The feasibility of using nutritional modifications to replace drugs in poultry feeds. Journal of Applied Poultry Research 11: 437–452.CrossRefGoogle Scholar
McCracken, K.J., Preston, C.M. and Butler, C. (2002) Effects of wheat variety and specific weight on dietary apparent metabolizable energy concentration and performance of broiler chicks. British Poultry Science 43: 253–260.Google Scholar
McDevitt, R.M., Brooker, J., Acamovic, T. and Sparks, N.H.C. (2005) The effect of non-starch polysaccharide inclusion in the diet on Clostridium perfringens in the gut of the broiler chicken. British Poultry Abstracts 1: 10–11.Google Scholar
Makkar, H.P.S. (2003) Quantification of tanins in tree and shrub foliage. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
McDonel, J.L. (1986) Toxins of Clostridium perfringens types A, B, C, D and E. In: Pharmacology of Bacterial Toxins. Dorner, F. and Drews, J. (Eds) Pergamon Press, Oxford Pp. 477–517.Google Scholar
Mellor, S. (2002) Enzymes make the grade. World Poultry 18(4): 26–28.Google Scholar
Morishita, Y., Oowada, T., Ozaki, A. and Mizutani, T. (2002) Galactooligosaccharide in combination with Bifidobacterium and Bacteroides affects the population of Clostridium perfringens in the intestine of gnotobiotic mice. Nutrition Research 22: 1333–1341.Google Scholar
Morrow, C. (2001) Solving the problems of necrotic enteritis. British Poultry Science 42: S65–S67.Google Scholar
McCartney, E. (2002) The natural world strikes back. Poultry International January Pp. 36–42.Google Scholar
McReynolds, J.L., Byrd, J.A., Anderson, R.C., Moore, R.W., Edrington, T.S., Genovese, K.J., Poole, T.L., Kubena, L.F. and Nisbet, D.J. (2004) Evaluation of immunosuppressants and dietary mechanisms in an experimental disease model for necrotic enteritis. Poultry Science 83: 1948–1952.Google Scholar
Miyata, S., Minami, J., Tamai, E., Matsushita, O., Shimamoto, S. and Okabe, A. (2002) Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. Journal of Biological Chemistry 277: 39463–39468.Google Scholar
Nisbet, D.J., Corrier, D.E., Scanlan, C.M., Hollister, A.G., Beier, R.C. and Deloach, J.R. (1993) Effect of a defined continuous flow-derived bacterial culture and dietary lactose on Salmonella typhimurium colonisation in broiler chickens. Avian Disease 37: 1017–1025.Google Scholar
Norton, R.A., Hopkins, B.A., Skeeles, J.K., Beasley, J.N. and Kreeger, J.M. (1992) High mortality of domestic turkeys associated with Ascaridi dissimilis. Avian Diseases 36: 469–473.Google Scholar
Novak, J.S. and Fratamico, P.M. (2004) Evaluation of ascorbic acid as a quorum-sensing analogue to control growth, sporulation, and enterotoxin production in Clostridium perfringens. Journal of Food Science 69: FMS72–FMS78.Google Scholar
Pedersen, K., Kaldhusdal, M., Engstrom, B., Engberg, R.M., Lovland, A., Nauerby, B. and Bjerrum, L. (2004) Clostridium perfringens: a lurking threat for poultry farming? Dansk Veterinaertidsskrift 87: 18–22.Google Scholar
Petit, L., Maier, E., Gibert, M., Popoff, M.R. and Benz, R. (2001) Clostridium perfringens epsilon toxin induces a rapid change of cell membrane permeability to ions and forms channels in artificial lipid bilayers. Journal of Biological Chemistry 276: 15736–15740.Google Scholar
Pirvulescu, M., Danes, M., Gruia, M., Ionita, C., Malinetescu, M., Panta, L., Popescu, V., Popovici, A., Simion-Gabor, M. and Tetu-Oporanu, M. (1999) Bioassays in HPCDIR and conventional piglets of the immunoamplifying properties of BIO-MOS (Alltech, USA), a probiotic. Studies and Researches in Veterinary Medicine 7: 51–65.Google Scholar
Phillips-Jones, M.K. (2000) Use of a lux reporter system for monitoring rapid changes in alpha -toxin gene expression in Clostridium perfringens during growth. FEMS Microbiology-Letters. 188: 29–33.Google Scholar
Porter, R.E. (1998) Bacterial enterides of poultry. Poultry Science 77: 1159–1165.Google Scholar
Prescott, J.F. (1979) The prevention of experimentally induced necrotic enteritis in chickens by avoparcin. Avian Diseases 23: 1072–1074.Google Scholar
Pusztai, A. and Bardocz, S. (1996) Biological effects of plant lectins on the gastrointestinal tract: Metabolic consequences and applications. Trends in Glycoscience and Glycotechnology 8: 149–165.Google Scholar
Ravdin, J.I., Murphy, C.F., Guerrant, R.L. and Long-Krug, S.A. (1985) Effect of antagonists of calcium and phospholipase A on the cytopathogenicity of Entamoeba histolytica. Journal of Infectious Diseases 152: 542–549.CrossRefGoogle ScholarPubMed
Reid, C.A. and Hillman, K. (1999) The effects of retrogradation and amylose/amylopectin ratio of starches on carbohydrate fermentation and microbial populations in the porcine colon. Animal Science 68: 503–510.Google Scholar
Riddle, C. and Kong, X. (1992) The influence of diet on necrotic enteritis in broiler chicks. Avian Disease 36: 499–503.Google Scholar
Roberfroid, M.B. (2005) Introducing inulin-type fructans. British Journal of Nutrition 93: S13–S25.Google Scholar
Robins, C. and Brooker, J.D. (2005) The effects of Acacia aneura feeding on abomasal and intestinal structure and function in sheep. Animal feed Science and Technology. Special edition – Phytochemicals and livestock, Brooker, J. and Acamovic, T. (Eds) 121: 205–215.Google Scholar
Rood, J.I. (1998) Virulence genes of Clostridium perfringens. Annual Review of Microbiology 52: 333–360.Google Scholar
Rood, J.I. and Cole, S.T. (1991) Molecular genetics and pathogenesis of Clostridium perfringens. Microbiological Reviews 55: 621–648.CrossRefGoogle ScholarPubMed
Ross Tech (1999) Necrotic enteritis and associated conditions in broiler chickens. World Poultry 15: 44–47.Google Scholar
Ruff, M.D., Reid, W.M. and Ryan, A.P. (1980) Anticoccidial activity of narasin in broiler chickens reared in floor pens. Poultry Science 59: 2008–2013.Google Scholar
Shane, S. and Van Der Sluis, W. (2002) Global disease update 2002: more problems to be solved. World Poultry 18: 28–31.Google Scholar
Shane, S.M., Gyimah, J.E., Harrington, K.S. and Snider, T.G. (1985) Etiology and pathogenesis of necrotic enteritis. Veterinary Research Communications 9: 269–287.CrossRefGoogle ScholarPubMed
Shane, S.M., Gymiah, J. and Ochoa, R. (1981) Inter-relationship of intestinal coccidiosis and necrotic enteritis. Journal of American Veterinary Medical Association 197: 270 (Abstract).Google Scholar
Siriken, B., Bayram, I. and Onol, A.G. (2003) Effects of probiotics: alone and in a mixture of Biosacc (R) plus Zinc Bacitracin on the caecal microflora of Japanese quail. Research in Veterinary Science 75: 9–14.Google Scholar
Spring, P., Wenk, C., Dawson, K.A. and Newman, K.E. (2000) The effects of dietary mannanoligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of salmonella-challenged broiler chicks. Poultry Science 79: 205–211.Google Scholar
Songer, J.G. (1996) Clostridial enteric diseases of domestic animals. Clinical Microbiology Reviews 9: 216–234.Google Scholar
Stanley, V.G., Gray, C., Daley, M., Krueger, W.F. and Sefton, A.E. (2004) An alternative to antibiotic-based drugs in feed for enhancing performance of broilers grown on Eimeria spp.-infected litter. Poultry Science 83: 39–44.Google Scholar
Stavric, S. (1992) Defined cultures and prospects. International Journal of Food Microbiology 15: 245–263.Google Scholar
Surai, P.F. (2002) Natural Antioxidants in Avian Nutrition and Production. Nottingham University Press, Nottingham UK.Google Scholar
Svihus, B. (2001) Research note: a consistent low starch digestibility observed in pelleted broiler chicken diets containing high levels of different wheat varieties. Animal Feed Science and Technology 92: 45–49.CrossRefGoogle Scholar
Svihus, B., Juvik, E., Hetland, H. and Krogdahl, A. (2004) Causes for improvement in nutritive value of broiler chicken diets with whole wheat instead of ground wheat. British Poultry Science 45: 55–60.Google Scholar
Svihus, B., Uhlen, A.K. and Harstad, O.M. (2005) Effect of starch granule structure, associated components and processing on nutritive value of cereal starch: Areview. Animal Feed Science and Technology In press.Google Scholar
Takeda, T., Fukata, T., Miyamoto, T., Sasai, K., Baba, E. and Arakawa, A. (1995) The effects of dietary lactose and rye on cecal colonization of Clostridium-perfringens in chicks. Avian Diseases 39: 375–381.Google Scholar
Tester, R.F., Karkalas, J. and Qi, X. (2004) Starch structure and digestibility. Enzyme substrate relationship. World's Poultry Science Journal 60: 186–195.Google Scholar
Titball, R.W. and Rood, J.I. (2002) Clostridium perfringens: wound infections. Molecular Medical Microbiology 1–3: 1875–1903.Google Scholar
Van Der Sluis, W. (2000) Clostridial enteritis is an often underestimated problem. World Poultry 16: 42–43.Google Scholar
Veterinary Medicines Directorate (2000) Sales of antimicrobial products used as veterinary medicines or growth promoters in the UK from 1993–1998. London U.K. 04 2000.Google Scholar
Veterinarymedicines Directorate (2002) Sales of antimicrobial products authorised for use as veterinary medicines, antiprotozoals, antifungals, growth promoters and coccidiostats in the UK in 2002. London U.K.06 2002.Google Scholar
Viera, S.L. (2003) Nutritional implications of mould development in feedstuffs and alternatives to reduce the mycotoxin problem in poultry feeds. World's Poultry Science Journal 59: 111–122.Google Scholar
Vissiennon, T., Menger, S. and Langhof, I. (1996) Hepatic and renal ultrastructural lesions in experimental Clostridium perfringens type Aenterotoxemia in chickens. Avian Diseases 40: 720–724.Google Scholar
Waldenstedt, L., Elwinger, K., Lunden, A., Thebo, P., Bedford, M.R. and Uggla, A. (2000) Intestinal digesta viscosity decreases during coccidial infection in broilers. British Poultry Science 41: 459–464.Google Scholar
Waterman, P.G. and Mole, S. (1994) Analysis of phenolic plant metabolites. Blackwell Scientific Publishing, Oxford U.K.Google Scholar
Waters, M., Savoie, A., Garmory, H.S., Bueschel, D., Popoff, M.R.Songer, J.G., Titball, R.W., Mcclane, B.A. and Sarker, M.R. (2003) Genotyping and phenotyping of beta2-toxigenic Clostridium perfringens fecal isolates associated with gastrointestinal diseases in piglets. Journal of Clinical Microbiology 41: 3584–3591.Google Scholar
Weurding, R.E, Veldman, A, Veen, A.M.G, Van Der Aar, P.J and Verstegen, M.W.A. (2001) Starch digestion in the small intestine of chickens differs among feedstuffs. Journal of Nutrition 131: 2329–2335.CrossRefGoogle ScholarPubMed
Wierup, M. (2001) The Swedish experience of the 1986 year ban of antimicrobial growth promotors, with special reference to animal health, disease prevention, productivity and usage of antimicrobials. Microbial Drug Resistance Mechanisms, Epidemiology and Disease 7: 183–190.Google Scholar
Willis, A.T. (1977) Anaerobic-bacteriology: clinical and laboratory practice. (3rd edition) Butterworths London. 360 pp .Google Scholar
Williams, R.B. (2005) Intercurrent coccidosis and necrotic enteritis of chickens; rational, integrated disease management by maintenance of gut integrity. Avian Pathology 34: 159–180.Google Scholar
Williams, R.B. (2002) Anticoccidial vaccines for broiler chickens: pathways to success. Avian Pathology 31: 317–353.Google Scholar
Williams, R.B., Marshall, R.N., Laragione, R.M. and Catchpole, J. (2003) Anew method for the experimental production of necrotic enteritis and its use for studies on the relationships between necrotic enteritis, coccidiosis and anticoccidial vaccination of chickens. Parasitology Research 90: 19–26.Google Scholar
Williams, B.A., Verstegen, M.W.A. and Tamminga, S. (2001) Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutrition Research Reviews 14: 207–227.Google Scholar
WORLD HEALTH ORGANISATION (W.H.O.) (1997) The medical impact of antimicrobial use in food animals. Who/Emc/Zoo/97.4. Report of a W.H.O. meetingBerlin Germany.Google Scholar
Xavier, K.B. and Bassler, B.L. (2003) LuxS quorum sensing: more than just a numbers game. Current Opinion in Microbiology 6: 191–197.Google Scholar
Youn-Heejeong, and Noh-Jaewuk, (2001) Screening of the anticoccidial effects of herb extracts against Eimeria tenella. Veterinary Parasitology 96: 257–263.Google Scholar
Zimmer, M., Vukov, N., Scherer, S. and Loessner, M.J. (2002) The murein hydrolase of the bacteriophage phi 3626 dual lysis system is active against all tested Clostridium perfringens strains. Applied and Environmental Microbiology 68: 5311–5317.Google Scholar