Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T03:30:32.214Z Has data issue: false hasContentIssue false
  • English
  • Français

Sub-clinical necrotic enteritis: its aetiology and predisposing factors in commercial broiler production

Published online by Cambridge University Press:  13 November 2014

M.W.C.D. PALLIYEGURU  and
S.P. ROSE
M.W.C.D. PALLIYEGURU*
Affiliation:
Harper Adams University, Newport, Shropshire, United Kingdom Veterinary Research Institute, P.O. Box 28, Peradeniya, Sri Lanka
S.P. ROSE
Affiliation:
Harper Adams University, Newport, Shropshire, United Kingdom
*
Corresponding author: [email protected]
Get access

Abstract

Sub-clinical necrotic enteritis (NE) is a major economic cost to the broiler production industry due to poor growth and feed conversion efficiency of broiler chicken flocks, higher condemnation of livers or rarely the whole carcasses at the slaughter house and an increased risk of microbial contamination of poultry meat. Sub-clinical NE is a multifactorial disease although Clostridium perfringens plays a major role in its pathogenesis. Its diagnosis and confirmation are quite different from those of general infectious diseases. Disease confirmation is from the presence of necrotic or ulcerative lesions on the small intestinal mucosa with identifiable aggregates of pathogenic C. perfringens. C. perfringens numbers in the small intestinal digesta or the mucosal scrapings are not correlated with disease severity, whereas counts above 106 cfu/g in the caecal contents indicate an increased probability of NE-specific gut lesions. Not only does the presence and counts of C. perfringens strains capable of producing related toxins affect the incidence of the disease but also a number of predisposing factors are important in the aetiology of NE. The major factors that predispose growing chickens to sub-clinical NE are diet variables, diseases that cause mucosal damage of the intestine and environmental factors that either alter the development of gut associated lymphoid tissue or change litter quality within the production house. Dietary variables may be a major cause of variation in sub-clinical NE in commercial broiler production; differences in polysaccharides, lipids, protein sources, protein digestibility and the presence of antinutritive factors have been identified as variables affecting the incidence of the disease.

Keywords

necrotic enteritisaetiologypredisposing factorssub-clinicalC. perfringensdietprotein
Type
Review Article
Information
World's Poultry Science Journal , Volume 70 , Issue 4 , December 2014 , pp. 803 - 816
Copyright
Copyright © World's Poultry Science Association 2014 

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.)

References

ABILDGAARD, L., SONDERGAARD, T.E., ENGBERG, R.M., SCHRAMM, A. and HØJBERG, O. (2010) In vitro production of necrotic enteritis toxin B, NetB, by netB-positive and netB-negative Clostridium perfringens originating from healthy and diseased broiler chickens. Veterinary Microbiology 144: 231-235.Google Scholar
AL-SHEIKHLY, F. and AL-SAIEG, A. (1980) Role of coccidiosis in the occurrence of necrotic enteritis of chickens. Avian Diseases 24: 324-333.Google Scholar
AL-SHEIKHLY, F. and TRUSCOTT, R.B. (1977a) The pathology of necrotic enteritis of chickens following Infusion of broth cultures of Clostridium perfringens into the duodenum. Avian Diseases 21: 230-240.Google Scholar
AL-SHEIKHLY, F. and TRUSCOTT, R.B. (1977b) 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
AL-SHEIKHLY, F. and TRUSCOTT, R.B. (1977c) The interaction of Clostridium perfringens and its toxins in the production of necrotic enteritis of chickens. Avian Diseases 21: 256-263.Google Scholar
ANNETT, C.B., VISTE, J.R., CHIRINO-TREJO, M., CLASSEN, H.L., MIDDLETON, D.M. and SIMKO, E. (2002) Necrotic enteritis: effect of barley, wheat and corn diets on proliferation of Clostridium perfringens type A. Avian Pathology 3: 599-602.Google Scholar
APAJALAHTI, J.H.A., KETTUNEN, A., BEDFORD, M.R. and HOLBEN, W.E. (2001) Percent G+C profiling accurately reveals diet-related differences in gastrointestinal microbial community of broiler chickens. Applied Environmental Microbiology 67: 5656-5667.Google Scholar
BANNAM, T.L., YAN, X., HARRISON, P.F., SEEMANN, T., KEYBURN, A.L., STUBENRAUCH, C., WEERAMANTRI, L.H., CHEUNG, J.K., MCCLANE, B.A., BOYCE, J.D., MOORE, R.J. and ROOD, J.I. (2011) Necrotic enteritis-derived Clostridium perfringens strain with three closely related independently conjugative toxin and antibiotic resistance plasmids. mBio. 2: e00190-11.Google Scholar
BARBARA, A.J., TRINH, H.T., GLOCK, R.D. and SONGER, J.G. (2008) Necrotic enteritis-producing strains of Clostridium perfringens displace non-necrotic enteritis strains from the gut of chicks. Veterinary Microbiology 126: 377-387.Google Scholar
BAR-SHIRA, E., SKLAN, D. and FRIEDMAN, A. (2003) Establishment of immune competence in the avian GALT during the immediate post-hatch period. Development and Comparative Immunology 27: 147-157.Google Scholar
BEDFORD, M.R. and CLASSEN, H.L. (1992) Reduction of intestinal viscosity through manipulation of dietary rye and pentosanase concentration is effected through changes in the carbohydrate composition of the intestinal aqueous phase and results in improved growth rate and food conversion efficiency of broiler chicks. Journal of Nutrition 122: 560-569.Google Scholar
BEN-NATHAN, B., DRABKIN, N. and HELLER, D. (1981) The effect of starvation on the immune response of chickens. Avian Diseases 25: 214-217.Google Scholar
BRANTON, S.L., REECE, F.N. and HAGLER-JR, W.M. (1987) Influence of a wheat diet on mortality of broiler chickens associated with necrotic enteritis. Poultry Science 66: 1326-1330.Google Scholar
BRANTON, S.L., LOTT, B.D., DEATON, J.W., MASLIN, W.R., AUSTIN, F.W., POTE, L.M., KEIRS, R.W., LATOUR, M.A. and DAY, E.J. (1997) The effect of added complex carbohydrates or added dietary fibre on necrotic enteritis lesions in broiler chickens. Poultry Science 76: 24-28.Google Scholar
CHALMERS, G., BRUCE, H.L., HUNTER, D.B., PARREIRA, V.R., KULKARNI, R.R., JIANG, Y.F., PRESCOTT, J.F. and BOERLIN, P. (2008) Multilocus sequence typing analysis of Clostridium perfringens isolates from necrotic enteritis outbreaks in broiler chicken populations. Journal of Clinical Microbiology 46: 3957-3964.Google Scholar
CHOCT, M. and ANNISON, G. (1992) The inhibition of nutrient digestion by wheat pentosans. British Journal of Nutrition 67: 123-132.Google Scholar
COLLETT, S.R. (2004) Controlling gastrointestinal disease to improve absorptive membrane integrity and optimize digestion efficiency, in: TUCKER, L.A. & TAYLOR-PICKARD, D.J.A. (Eds) Interfacing Immunity, Gut Health and Performance, pp. 77-92 (Nottingham, Nottingham University Press).Google Scholar
COOPER, K.K. and SONGER, J.G. (2010) Virulence of Clostridium perfringens in an experimental model of poultry necrotic enteritis. Veterinary Microbiology 142: 323-328.CrossRefGoogle Scholar
CRAVEN, S.E. (2000) Colonisation of the intestinal tract by Clostridium perfringens and faecal shedding in the diet-stressed and unstressed broiler chickens. Poultry Science 79: 843-849.Google Scholar
CRAVEN, S.E., STERN, N.J., BAILEY, S.J. and COX, N.A. (2001) Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Diseases 45: 887-896.Google Scholar
CRESPO, R., FISHER, D.J., SHIVAPRASAD, H.L., FERNANDEZ-MIYAKAWA, M.E. and UZAL, F.A. (2007) Toxinotypes of Clostridium perfringens isolated from sick and healthy avian species. Journal of Veterinary Diagnostic Investigation 19: 329-333.CrossRefGoogle ScholarPubMed
DAHIYA, J.P., WILKIE, D.C., VAN KESSEL, A.G. and DREW, M.D. (2006) Potential strategies in broiler chickens in post-antibiotic era. Animal Feed Science and Technology 129: 60-88.Google Scholar
DAS, A., MAZUMDER, Y., DUTTA, B.K., SHOME, B.R., BUJARBARUAH, K.M. and KUMAR, A. (2008) Clostridium perfringens type A from broiler chicken with necrotic enteritis. International Journal of Poultry Science 7: 601-609.Google Scholar
DREW, M.D., SYED, N.A., GOLDADE, B.G., LAARVELD, B. and VAN KESSEL, A.G. (2004) Effect of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens. Poultry Science 83: 414-420.Google Scholar
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., BERNDTSON, E., ENGSTOM, B., FOSSUM, O. and WALDENSTEDT, L. (1998) Effect of antibiotic growth promoters and anticoccidials on growth of Clostridium perfringens in the caeca and on performance of broiler chickens. Acta Veterinaria Scandinavica 39: 433-441.Google Scholar
ENGSTROM, B.E., FERMER, C., LINDBERG, A., SAARINEN, E., BAVERUD, V. and GUNNARSSON, A. (2003) Molecular typing of Clostridium perfringens from healthy and diseased poultry. Veterinary Microbiology 94: 225-235.CrossRefGoogle ScholarPubMed
FERNANDO, P.S., ROSE, S.P., MACKENZIE, A.M. and SILVA, S.S.P. (2011) Effect of diets containing potato protein or soya bean meal on the incidence of spontaneously occurring sub-clinical NE crotic enteritis and the physiological response in broiler chickens. British Poultry Science 52: 106-114.CrossRefGoogle ScholarPubMed
GARRIDO, M.N., SKJERVHEIM, M.H., OPPEGAARD, H. and SØRUM, H. (2004) Acidified litter benefits the intestinal flora balance of broiler chickens. Applied Environmental Microbiology 70: 5208-5213.CrossRefGoogle ScholarPubMed
GHOLAMIANDEKHORDI, A.R., DUCATELLE, R., HYNDRICKX, M., HAESEBROUCK, F. and VAN IMMERSEEL, F. (2006) Molecular and phenotypical characterisation of Clostridium perfringens isolates from poultry flocks with different disease status. Veterinary Microbiology 113: 143-152.Google Scholar
GIOVANNINI, C., MANCINI, E. and DE VINCENZI, M. (1996) Inhibition of the cellular metabolism of Caco-2 cells by prolamin peptides from cereals toxic for coeliacs. Toxicology In Vitro 10: 533-538.CrossRefGoogle ScholarPubMed
GOHL, B. and GOHL, I. (1977) The effect of viscous substances on the transit time of the Barley digesta in rats. Journal of the Science of Food and Agriculture 28: 911-915.Google Scholar
GRANUM, P.E. and PECK, M.W. (2006) Methods for use with food poisoning Clostridia, in: MAINIL, J., DUCHESNES, C., GRANUM, P.E., MENOZZI, M.G., PECK, M., PELKONEN, S., POPOFF, M., STACKEBRANDT, E. & TITBALL, R. (Eds) Genus Clostridium: Clostridia in medical, veterinary and food microbiology diagnosis and typing, pp. 188-198 (Luxembourg: Office for Official Publications of the European Communities).Google Scholar
GUTIERREZ, J., BARRY-RYAN, C. and BOURKE, P. (2008) The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. International Journal of Food Microbiology 124: 91-97.Google Scholar
HERMANS, P.G. and MORGAN, K.L. (2007) Prevalence and associated risk factors of necrotic enteritis on broiler farms in the United Kingdom; across-sectional survey. Avian Pathology 36: 43-51.CrossRefGoogle Scholar
INAGAKI, T., MOSCHETTA, A., LEE, Y.K., PENG, L., ZHAO, G., DOWNES, M., YU, T., SHELTON, J.M., RICHARDSON, J.A., REPA, J.J., MANGELSDORF, D.J. and KLIEWER, S.A. (2006) Regulation of antibacterial defence in the small intestine by the nuclear bile acid receptor. Proceedings of the National Academy of Science of the USA (PNAS) 103: 3920-3925.Google Scholar
JADHAV, S.J. and KADAM, S.S. (1998) Potato, in: SALUNKHE, D.K. & KADAM, S.S. (Eds) Handbook of Vegetable Science and Technology, Production, Composition, Storage, and Processing, pp. 11-69 (New York, Marcel Dekker Inc).Google Scholar
JOHANSSON, A. (2006) Clostridium perfringens the causal agent of necrotic enteritis in poultry. Ph.D. Thesis, Swedish University of Agricultural Sciences, Uppsala.Google Scholar
JOHNSON, D.C. and PINEDO, C. (1971) Gizzard erosion and ulceration in Peru broilers. Avian Diseases 15: 835-837.Google Scholar
JOHNSON, I.T. and GEE, J.M. (1981) Effect of gel-forming gums on the intestinal unstirred layer and sugar transport in vitro. Gut 22: 398-403.Google Scholar
KAHN, C.M. and LINE, S. (2005) The Merck Veterinary Manual 9th ed. pp. 2185-2336 (Whitehouse Station, NJ, USA: Merck and Co. Inc.)Google Scholar
KALDHUSDAL M.I. (2000) Necrotic enteritis as affected by dietary ingredients. World Poultry 16: 42-43.Google Scholar
KALDHUSDAL, M.I. and HOFSHAGEN, M. (1992) Barley inclusion and avoparcin supplementation in broiler diets. 2. Clinical pathological and bacteriological findings in a mild form of Necrotic Enteritis. Poultry Science 71: 1145-1153.CrossRefGoogle Scholar
KALDHUSDAL, M.I. and SKJERVE, E. (1996) Association between cereal contents in the diet and incidence of necrotic enteritis in broiler chickens in Norway. Preventive Veterinary Medicine 28: 1-16.Google Scholar
KALDHUSDAL, M.I., HOFSHAGEN, M., LOVLAND, A., LANGSTRAND, H. and REDHEAD, K. (1999) 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
KEYBURN, A.L., BOYCE, J.D., VAZ, P., BANNAM, T.L., FORD, M.E. and PARKER, D. (2008) NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathogens 4: e26-11.Google Scholar
KNARREBORG, A., SIMON, M.A., ENGBERG, R.M., JENSEN, B.B. and TANNOCK, G.W. (2002a) Effect of dietary fat source and sub-therapeutic levels of antibiotic on the bacterial community in the ileum of broiler chickens. Applied and Environmental Microbiology 68: 5918-5924.CrossRefGoogle Scholar
KNARREBORG, A., ENGBERG, R.M., JENSEN, S.K. and JENSEN, B.B. (2002b) Quantitative determination of bile salt hydrolase activity in bacteria isolated from the small intestine of chickens. Applied and Environmental Microbiology 68: 6425-6428.Google Scholar
KULKARNI, R.R., PARREIRA, V.R., SHARIF, S. and PRESCOTT, J.F. (2007) Immunisation of broiler chickens against Clostridium perfringens-induced necrotic enteritis. Clinical and Vaccine Immunology 14: 1070-1077.Google 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.Google Scholar
LOVLAND, 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
MANSSON, I. and OLHAGEN, B. (1967) Intestinal Clostridium perfringens in arthritis and parakeratosis induced by dietary factors. Experimental studies in pigs. Bulletin de l'Office International des Epizooties 61: 1319-1327.Google Scholar
MARTIN, T.G. and SMYTH, J.A. (2010) The ability of disease and non-disease producing strains of Clostridium perfringens from chickens to adhere to extracellular matrix molecules and Caco-2 cells. Anaerobe 16: 533-539.Google Scholar
MCCLANE, B.A. (1997) Clostridium perfringens, in: DOYLE, M.P., BEUCHAT, L.R. & MONTVILLE, T.J. (Eds) Food Microbiology: Fundamentals and Frontiers, pp. 305-326 (Washington, DC, ASM Press).Google Scholar
MCDEVITT, R.M., BROOKER, J.D., ACAMOVIC, T. and SPARKS, N.H.C. (2006) Necrotic enteritis; a continuing challenge for the poultry industry. World's Poultry Science Journal 62: 221-247.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: 1984-1952.Google Scholar
MITSCH, P., ZITTERL-EGLSEER, K., KOHLER, B., GABLER, C., LOSA, R. and ZIMPERNIK, I. (2004) The effect of two different blends of essential oil components on the proliferation of Clostridium perfringens in the intestines of broiler chickens. Poultry Science 83: 669-675.Google Scholar
NAIRAN, M.E. and BAMFORD, V.W. (1967) Necrotic enteritis of broiler chickens in Western Australia. Australian Veterinary Journal 43: 49-54.Google Scholar
NAUERBY, B., PEDERSEN, K. and MADSEN, M. (2003) Analysis by pulsed field gel electrophoresis of the genetic diversity among Clostridium perfringens isolates from chickens. Veterinary Microbiology 94: 257-266.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 Ascaridia dissimilis. Avian Diseases 36: 469-473.Google Scholar
OLKOWSKI, A.A., WOJNAROWICZ, C., CHIRINO-TREJO, M. and DREW, M.D. (2006) Responses of broiler chickens orally challenged with Clostridium perfringens isolated from field cases of necrotic enteritis. Research in Veterinary Science 81: 99-108.Google Scholar
PALLIYEGURU, M.W.C.D. and ROSE, S.P. (2009) The pathology and proposed pathogenesis of sub-clinical necrotic enteritis spontaneous disease model simulating the conditions in the broiler industry. Book of abstracts XVI World Veterinary Poultry Association Congress, Marrakech, Morocco, pp.180.Google Scholar
PALLIYEGURU, M.W.C.D., ROSE, S.P. and MACKENZIE, A.M. (2010) Effect of dietary protein concentrates on the incidence of sub-clinical necrotic enteritis and growth performance of broiler chickens. Poultry Science 89: 34-43.CrossRefGoogle Scholar
PALLIYEGURU, M.W.C.D., ROSE, S.P. and MACKENZIE, A.M. (2011) Effect of trypsin inhibitor activity in soya bean on the growth performance, protein digestibility and incidence of sub-clinical necrotic enteritis in broiler chicken flocks. British Poultry Science 52: 359-367.Google Scholar
PARK, S.S., LILLEHOJ, H.S., ALLEN, P.C., PARK, D.W., FITZCOY, S., BAUTISTA, D.A. and LILLEHOJ, E.P. (2008) Immunopathology and cytokine responses in broiler chickens coinfected with Eimeria maxima and Clostridium perfringens with the use of an animal model of necrotic enteritis. Avian Diseases 52: 14-22.Google Scholar
PEDERSEN, K., BJERRUM, L. HEUER, O.E. WONG, D.M.A.L.F. and NAUERBY, B. (2008) Reproducible infection model for Clostridium perfringens in broiler chickens. Avian Diseases 52: 34-39.Google Scholar
QUINN, P.J., CARTER, M.E., MARKEY, B.K. and CARTER, G.R. (1994) Clostridium species, in: Clinical Veterinary Microbiology, pp. 191-208 (London, Wolfe Publishing).Google Scholar
QUINN, P.J., MARKEY, B.K., CARTER, M.E., DONNELLY, W.J. and LEONARD, F.C. (2002) Veterinary Microbiology and Microbial diseases, pp. 85-95 (Oxford, Blackwell Science Ltd).Google Scholar
RAO, B.G.V.N. and NIGAM, S.S. (1970) The in vitro antimicrobial efficiency of essential oils. Indian Journal of Medical Research 58: 627-633.Google Scholar
SCHRADER, J., BROUSSARD, C., HANSEN, J., DIERKS, L., OETTING, A. and PETERSEN, G. (2008) Association of Clostridium perfringens type A alpha-toxin with lesions of necrotic enteritis evaluated by monoclonal antibody test strips and immunohistochemistry. Proceedings of World's Poultry Congress XXIII Brisbane, Australia, pp. 14-17.Google Scholar
SHANE, S.M., GYIMAH, J.E., HARRINGTON, K.S. and SNIDER, T.G. (1985) Aetiology and pathogenesis of necrotic enteritis. Veterinary Research Communications 9: 269-287.Google Scholar
SHIVARAMAIAH, S., WOLFENDEN, R.E., BARTA, J.R., MORGAN, M.J., WOLFENDEN, A.D., HARGIS, B.M. and TÉLLEZ, G. (2011) The role of an early Salmonella Typhimurium infection as a predisposing factor for necrotic enteritis in a laboratory challenge model. Avian Diseases 55: 319-323.Google Scholar
SMITH, D.B., RODDICK, J.G. and JONES. J.L. (1996) Potato glycoalkaloids: some unanswered questions. Trends in Food Science and Technology 7: 126-131.CrossRefGoogle Scholar
SMITH, E.A. and MACFARLANE, G.T. (1998) Enumeration of amino acid fermenting bacteria in the human large intestine: effect of pH and starch on peptide metabolism and dissimilation of amino acids. FEMS Microbiology Ecology 25: 355-368.Google Scholar
STEVENS, D.L. and BRYANT, A.E. (2002) The role of Clostridial toxins in the pathogenesis of gas gangrene. Clinical Infectious Diseases 35: S93-S100.CrossRefGoogle ScholarPubMed
STEVENS, D.L. and ROOD, J.I. (2006) Histotoxic Clostridia, in: FISCHETTI, E.A. (Ed.) Gram-Positive Pathogens, 2nd ed., pp. 715-725 (Washington D.C, ASM press).Google Scholar
UNTAWALE, G.G., PIETRASZEK, A. and MCGINNIS, J. (1978) Effect of diet on adhesion and invasion of microflora in the intestinal mucosa of chicks. Proceedings of the Society for Experimental Biology and Medicine 159: 276-280.Google Scholar
VAHOUNY, G.V. and CASSIDY, M.M. (1986) Dietary fibre and intestinal adaptation, in: VAHOUNY, G.V. & DRITCHEVSKY, D. (Eds) Dietary Fibre: Basic and Clinical Aspects, pp. 181-209 (New York, Plenum Press).Google Scholar
VAN DIJK, J.E., HUISMAN, J. and KONINKX, J.F.J.G. (2002) Structural and functional aspects of a healthy gastrointestinal tract, in: BLOK, M.C., VAHL, H.A., DE LANGE, L., VAN DE BRAAK, A.E., HEMKE, G. & HESSING, M. (Eds) Nutrition and Health of the Gastrointestinal tract, pp. 71-96. (Wageningen, Wageningen Academic Publishers).Google Scholar
WAGES, D.P. and OPENGART, K. (2003) Necrotic Enteritis, in: SAIF, Y.M. (Ed.) Diseases of Poultry, 11th ed., pp. 781-785 (Iowa, Iowa state press).Google Scholar
WIDYARATNE, G.P. (2012) The role of protein and amino acid nutrition in controlling clostridium perfringens in the gastrointestinal tract of broiler chickens. Ph.D. Thesis, University of Saskatchewan.Google Scholar
WILLIAMS, R.B. (2005) Review Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathology 34: 159-180.Google Scholar
WILLIAMS, R.B., MARSHALL, R.N., LA RAGIONE, R.M. and CATCHPOLE, J. (2003) A new 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
YITBAREK, A., ECHEVERRY, H., BRADY, J., ERNANDEZ-DORIA, J., CAMELO-JAIMES, G., SHARIF, S., GUENTER, W., HOUSE, J.D. and RODRIGUEZ-LECOMPTE, J.C. (2012) Innate immune response to yeast-derived carbohydrates in broiler chickens fed organic diets and challenged with Clostridium perfringens. Poultry Science 91: 1105-1112.Google Scholar
ZENTEK, J., VAN DER STEEN, ROHDE, J. and AMTSBERG, G. (1998) Dietary effects on the occurrence and enterotoxin production of Clostridium perfringens in the canine gastrointestinal tract. Journal of Animal Physiology 80: 250-252.Google Scholar