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Manifestations of Clostridium perfringens and related bacterial enteritides in broiler chickens

Published online by Cambridge University Press:  18 September 2007

J. Wilson
Affiliation:
Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
G. Tice
Affiliation:
Elanco Animal Health, Division of Eli Lilly and Co., Greenfield, IN
M. L. Brash*
Affiliation:
Elanco, Division Eli Lilly Canada Inc., Guelph, Ontario, Canada
S. St. Hilaire
Affiliation:
Idaho State University, Pocatello, ID
*
*Corresponding author: [email protected]
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Abstract

Well known as the cause of necrotic enteritis, C. perfringens (CP) is now recognized as causing a spectrum of effects including subclinical infection, mild disease with focal intestinal necrosis, diarrhoeal illness and liver disease, as well as the classic form of acute fulminant necrotizing enteritis. The mild and subclinical forms of infection appear to be widespread, and, possibly increasing in incidence. Furthermore, bacterial enteritis is increasingly being recognized less as an invasion by pathogenic organisms per se and more as an expression of the normal process by which the intestinal bacterial population changes overtime in response to changes in the intestinal environment. Such shifts in enteric bacterial populations have been referred to as dysbacteriosis. Management of the microbial ecology of the intestinal tract is therefore an important element of preventing disease, enhancing performance, and preventing foodborne illness. Diagnosis of emerging forms of bacterial enteritis including CP infection can be challenging and involves a comprehensive analysis of flock history and condemnation records, clinical signs, gross and histopathology, bacterial culture and empirical response to treatment, augmented by molecular techniques where available. Control measures are at present based on extensions of validated approaches to the control of the classical form of the disease: managing known risk factors for necrotic enteritis (coccidiosis, diet and litter quality) and the use of approved antimicrobial agents with proven efficacy against CP.

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Copyright © Cambridge University Press 2005

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References

Abrams, G.D., Bauer, H. and Sprintz, H. (1963) Influence of the normal flora on mucosal morphology and cellular renewal. A comparison of germ-free and conventional mice. Laboratory Investigation 12: 355364.Google ScholarPubMed
Al-Sheikhly, F. and Truscott, R.B. (1977a) The interaction of Clostridium perfringens and its toxins in the production of necrotic enteritis of chickens. Avian Diseases 21:(2): 256263.CrossRefGoogle ScholarPubMed
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(2): 241255.CrossRefGoogle ScholarPubMed
Al-Sheikhly, F. and Truscott, R.B. (1977c) The pathology of necrotic enteritis of chickens following infusion of broth cultures of Clostridium perfringens into the duodenum. Avian Diseases 21(2): 230240.CrossRefGoogle ScholarPubMed
Al-Sheikhly, F. and Al-Saieg, A. (1980) Role of coccidia in the occurrence of necrotic enteritis of chickens. Avian Diseases 24(2): 324333.CrossRefGoogle ScholarPubMed
Anderson, D.B., Mccracken, V.J., Aminov, R.I., Simpson, J.M., Mackie, R.I., Verstegen, M.W.A. and Gaskins, H.R. (2000) Gut microbiology and growth-promoting antibiotics in swine. Nutritional Abstracts and Reviews Series B: Livestock Feeds and Feeding 70(2): 102107.Google Scholar
Apajalahti, J.H.A., Sarkilahti, L.K., Maki, B.R.E., Heikkinen, J.P., Nurminen, P.H. and Holben, W.E. (1998) Effective recovery of bacterial DNA and percent-guanine-plus cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Applied and Environmental Microbiology 64: 40844088.CrossRefGoogle ScholarPubMed
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: 5962.CrossRefGoogle ScholarPubMed
Barker, I.K. and Van Dreumel, A.A. (1993) Intestine. Pages 1–318 in Pathology of Domestic Animals (4th Edition) Jubb, K.V.F.Kennedy, P.C. and Palmer, N. eds. Academic Press, Orlando FL.Google Scholar
Barnes, E.M., Mead, G.C., Barnum, D.A. and Harry, E.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: 311326.CrossRefGoogle Scholar
Barona, E., Julkunen, R., Tannenbaum, L. and Lieber, C.S. (1986) Role of intestinal bacterial overgrowth in ethanol production and metabolism in rats. Gastroenterology 90(1): 103110.CrossRefGoogle Scholar
Benno, Y., Endo, K. and Mitsuoka, T. (1988) Isolation of faecal Clostridium perfringens from broiler chickens and their susceptibility to eight antimicrobial agents for growth promotion. Japanese Journal of Veterinary Science 50(3): 832834.Google ScholarPubMed
Bernier, G., Filion, R.Malo, R. and Phaneuf, J-B. (1974a) Entérite nécrotique chez le poulet de gril II. Caractères des souches de Clostridium perfringens isolées. Canadian Journal of Comparative Medicine 38: 286291.Google Scholar
Bernier, G., Phaneuf, J-B. and Filion, R. (1974b) Entérite nécrotique chez le poulet de gril. I Aspect clinico-pathologique. Canadian Journal of Comparative Medicine 38: 280285.Google Scholar
Bernier, G., Phaneuf, J-B. and Filion, R. (1977) Entérite nécrotique chez le poulet de gril. III Étude des facteurs favorisant la multiplication de Clostridium perfringens et la transmission expérimentale de la maladie. Canadian Journal of Comparative Medicine 41: 112116.Google Scholar
Branton, S.L., Reece, F.N. and Hagler, W.M. (1987) Influence of a wheat diet on mortality of broiler chickens associated with necrotic enteritis. Poultry Science 66: 13261330.CrossRefGoogle ScholarPubMed
Branton, S.L., Lott, B.D., May, J.D., Hedin, P.A., Austin, F.W., Latour, M.A. and Days, E.J. (1996) The effects of nonautoclaved and autoclaved water-soluble wheat extracts on the growth of Clostridium perfringens. Poultry Science 75: 335338.CrossRefGoogle ScholarPubMed
Brennan, J., Moore, G., Poe, S.E., Zimmermann, A., Vessie, G., Barnum, D.A. and Wilson, J. (2001a) Efficacy of in-feed tylosin phosphate for the treatment of necrotic enteritis in broiler chickens. Poultry Science 80: 14511454.CrossRefGoogle ScholarPubMed
Brennan, J., Bagg, R., Barnum, D., Wilson, J. and Dick, P. (2001b) Efficacy of narasin in the prevention of necrotic enteritis in broiler chickens. Avian Diseases 45: 210214.CrossRefGoogle ScholarPubMed
Bunyan, J., Jeffries, L., Sayers, J.R., Gulliver, A.L. and Coleman, K. (1977) Antimicrobial substances and chick growth promotion: the growth-promoting activities of antimicrobial substances including fifty-two used either in therapy or as dietary additives. British Poultry Science 18: 283294.CrossRefGoogle Scholar
Carrier, D. (2000) Clostridial enteritis global impact assessment and global MIC survey – a review. Pages 56–75 in Proceedings of the Poultry Enteritis ConferenceElanco Animal Health, Montreal Que.Google Scholar
Casewell, M., Friis, C., Marco, E., Mcmullin, P. and Phillips, I. (2003) The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. Journal of Antimicrobial Chemotherapy 52: 159161.CrossRefGoogle ScholarPubMed
Coates, M.E. (1980) The gut microflora and growth. Pages 175–188 in Growth in Animals. Lawrence, T. L. J. ed. Butterworths, Boston MA.Google Scholar
Cole, C.B. and Fuller, R. (1984) Bile acid deconjugation and attachment of chicken gut bacteria: their possible role in growth depression. British Poultry Science 25: 227231.CrossRefGoogle ScholarPubMed
Collier, C.T., Van Der Kliss, J.D., Deplancke, B., Anderson, D.B. and Gaskins, H.R. (2003). Effects of Tylosin on bacterial mucolysis, Clostridium perfringens colonization, and intestinal barrier function in a chick model of necrotic enteritis. Antimicrobial Agents and Chemotherapy 47: 33113317.CrossRefGoogle Scholar
Cowen, B.S., Schwartz, L.D., Wilson, R.A. and Ambrus, S.I. (1987) Experimentally induced necrotic enteritis in chickens. Avian Diseases 31: 904906.CrossRefGoogle ScholarPubMed
Davison, T.F. and Freeman, B.M. (1983) Physiological aspects of growth promotion in poultry. Veterinary Research Communications 7: 5968.CrossRefGoogle ScholarPubMed
Deichmann, W.B. and Witherup, S. (1943) Phenol studies VI. The acute and comparative toxicity of phenol, o-, m-, and p-cresols for experimental animals. Journal of Pharmacology and Experimental Therapeutics 80: 223239.Google Scholar
Dudley-Cash, W. (2003) Field research measures effect of removing GPAfrom broiler feeds. Feedstuffs 10–12.Google Scholar
Dumitrasco, D., Grigoresco, M., Parau, N., Suciu, A. and Erdosy, S. (1980) Dysbacteriosis in enteropathies. Medecine Interne 18(3): 239245.Google ScholarPubMed
Dutta, G.N. and Devriese, L.A. (1980) Susceptibility of Clostridium perfringens of animal origin to fifteen antimicrobial agents. Journal of Veterinary Pharmacology and Therapeutics 3: 227236.CrossRefGoogle Scholar
Desomer, P., Eyssen, H. and Evrard, E. (1963) The influence of antibiotics on faecal fat in chicks. Pages 84–90 in Biochemical Problems of Lipids. Frazer, A.C. ed. Elsevier/North Holland Publishing Co., Amsterdam.Google Scholar
Eshuis, J.W., Van Dobbenburgh, O.A., Delhaes, L.M., Van Der Meij, D. and Nijland, J.T. (1998) Bacterie-regelaar Tylan an helpt tegen dysbacteriose. Pluimveehouderij 13.Google Scholar
Feighner, S.D. and Dashkevitz, M.P. (1987) Subtherapeutic levels of antibiotics in poultry feeds and their effects on weight gain, feed efficiency and bacterial cholytaurine hydrolase activity. Applied and Environmental Microbiology 53(2): 331336.CrossRefGoogle Scholar
Ficken, M.D. and Wages, D.P. (1997) Necrotic enteritis. Pages 261–264 in Diseases of Poultry 10th Edition. Calnek, B. W. ed. Iowa State Press Ames.Google Scholar
Floch, M.H., Binder, H.J., Filburn, B. and Gershengoren, W. (1972) The effects of bile acids on intestinal microflora. American Journal of Clinical Nutrition 25: 14181426.CrossRefGoogle ScholarPubMed
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(3): 601602.CrossRefGoogle ScholarPubMed
Fukata, T., Hadate, Y., Baba, E. and Arakawa, A. (1991) Influence of bacteria on Clostridium perfringens infections in young chickens. Avian Diseases 35: 224227.CrossRefGoogle ScholarPubMed
Gazdzinski, P. and Julian, R.J. (1992) Necrotic enteritis in turkeys. Avian Diseases 36: 792798.CrossRefGoogle ScholarPubMed
Gaskins, H.R. (1996) Immunological aspects of host/microbiota interactions at the intestinal epithelium. Pages 537–587 in Gastrointestinal Microbiology (vol.2) Gastrointestinal Microbes and Host Interactions. Mackie, R. I.White, B. A. and Isaacson, R. E. eds. Chapman and Hall, New York.Google Scholar
George, B.A., Quarles, C.L. and Fagerberg, D.J. (1982) Virginiamycin effects on controlling necrotic enteritis infection in chickens. Poultry Science 61: 447450.CrossRefGoogle ScholarPubMed
Gracey, M., Cullity, G.J. and Suharjono, S. (1977) The stomach in malnutrition. Archives of Disease in Childhood 52: 325327.CrossRefGoogle ScholarPubMed
Hamdy, A.H., Thomas, R.W., Yancey, R.J. and Davis, R.B. (1983) Therapeutic effect of optimal lincomycin concentration in drinking water on necrotic enteritis in broilers. Poultry Science 62: 589591.CrossRefGoogle ScholarPubMed
Henry, P.R., Ammerman, C.B. and Miles, R.D. (1986) Influence of virginiamycin and dietary manganese on performance, manganese utilization, and intestinal tract weight of broilers. Poultry Science 65: 321324.CrossRefGoogle ScholarPubMed
Henry, P.R., Ammerman, C.B., Campbell, D.R. and Miles, R.D. (1987) Effects of antibiotics on tissue trace mineral concentration and intestinal tract weight of broiler chicks. Poultry Science 66: 10141018.CrossRefGoogle ScholarPubMed
Hofshagen, M. and Kaldhusdal, M. (1992) Barley inclusion and avoparcin supplementation in broiler diets. 1. Effect on small intestinal bacterial flora and performance. Poultry Science 71: 959969.CrossRefGoogle ScholarPubMed
Hoitink, H. (1997) Clostridium infection is changing appearance. Pluimveehouderij 34.Google Scholar
Hoppe, P. (September), (1999) Wet Litter in broilers. Poultry International 52–62.Google Scholar
Hutchison, T.W.S. and Riddell, C. (1990) Astudy of hepatic lesions in broiler chickens at processing plants in Saskatchewan. Canadian Veterinary Journal 31: 2025.Google Scholar
Johnston, K.L. (1999) Small intestinal bacterial overgrowth. Progress in Gastroenterology 29(2): 523550.Google ScholarPubMed
Kaldhusdal, M. 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: 11451153.CrossRefGoogle Scholar
Kaldhusdal, M., Hofshagen, M., Lovland, A., Langstrand, A.H. and Redhead, K. (1999) Necrotic enteritis models with broiler chickens raised on litter: evaluation of preconditions, Clostridium perfringens strains and outcome variable. FEMS Immunology and Medical Microbiology 24(3): 337343.CrossRefGoogle Scholar
Kaldhusdal, M. and Lovland, A. (2002) Clostridial necrotic enteritis and cholangiohepatitis. Pages G3-G13 in Proceedings from The Elanco Global Enteritis Symposium.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. Preventive Veterinary Medicine 28: 116.CrossRefGoogle Scholar
King, C.E. and Toskes, P.P. (1979) Small intestine bacterial overgrowth. Gastroenterology 76: 10351055.CrossRefGoogle ScholarPubMed
Klemparskaya, N.N., Pinegin, B.V., Shal'nova, G.A., Korshunov, V.M., Mal'tsev, V.N., Glad'ko, I.A., Kuz'mina, T.D., Ulanova, A.M., Dobronravova, N.N. and Yermolov, V.V. (1987) Normalizing effect of immunoglobulins in the treatment of endogenous infection and intestinal dysbacteriosis in irradiated mice. Journal of Hygiene, Epidemiology, Microbiology and Immunology 31(1): 9198.Google ScholarPubMed
Kondo, F. (1988) In vitro lecithinase activity and sensitivity to 22 antimicrobial agents on Clostridium perfringens isolated from necrotic enteritis of broiler chickens. Research in Veterinary Science 45: 337340.CrossRefGoogle ScholarPubMed
Lee, M. (2002) Microbial dynamics of the broiler intestinal tract. Pages A1-A14 in Proceedings of the Poultry Enteritis ConferenceElanco Animal HealthCambridge, England.Google Scholar
Lichtman, S., Sherman, P. and Forstner, G. (1986) Production of secretory immunoglobulins Ain rat self-filling blind loops: Local secretory immunoglobulin A immune response to luminal bacterial flora. Gastroenterology 91: 14951502.CrossRefGoogle Scholar
Lichtman, S.N., Sartor, R.B., Keku, J. and Schwab, J.H. (1990) Hepatic inflammation in rats with experimental small intestinal bacterial overgrowth. Gastroenterology 98(2): 414423.CrossRefGoogle ScholarPubMed
Long, J.R. (1973) Necrotic enteritis in broiler chickens. I. Areview of the literature and the prevalence of the disease in Ontario. Canadian Journal of Comparative Medicine 37: 302308.Google Scholar
Long, J.R., Pettit, J.R. and Barnum, D.A. (1974) Necrotic enteritis in broiler chickens. II. Pathology and proposed pathogenesis. Canadian Journal of Comparative Medicine 38: 467474.Google ScholarPubMed
Long, J.R. and Truscott, R.B. (1976) Necrotic enteritis in broiler chickens. III. Reproduction of the disease. Canadian Journal of Comparative Medicine 40: 5359.Google Scholar
Lovland, A. and Kaldhusdal, M. (1999) Liver lesions seen at slaughter as an indicator of necrotic enteritis in broiler flocks. FEMS Immunology and Medical Microbiology 24(3): 345351.CrossRefGoogle ScholarPubMed
Lovland, A. and Kaldhusdal, M. (2001) Severely impaired production performance in broiler flocks with high incidence of Clostridium perfringens-associated hepatitis. Avian Pathology 30: 7381.CrossRefGoogle ScholarPubMed
Marsh, T.L. (1999) Terminal restriction fragment length polymorphism (T-RFLP): an emerging method for characterizing diversity among homologous populations of amplification products. Current Opinion in Microbiology 2: 323327.CrossRefGoogle ScholarPubMed
Mcdougald, L.R. (2003) Coccidiosis. Pages 974–991 in Diseases of Poultry 11th Edition. Saif, Y.M. ed. Iowa State Press Ames.Google Scholar
Mcmeekin, T.A., Brown, J., Krist, K., Miles, D., Neumeyer, K., Nichols, D. S., Olley, J., Presser, K., Ratkowsky, D.A., Ross, T., Salter, M. and Soontranon, S. (1997) Quantitative microbiology: a basis for food safety. Emerging Infectious Diseases 3(4): 541549.CrossRefGoogle ScholarPubMed
Mead, G.C. (1989) Microbes of the avian cecum: types present and substrates utilized. Journal of Experimental Zoology Supplement 3: 4854.CrossRefGoogle ScholarPubMed
Mortimer, I. (2002). The detection of dysbacteriosis. Pages D3-D7 in Proceedings from The Elanco Global Enteritis Symposium.Google Scholar
Netherwood, T., Gilbert, H.J., Parker, D.S. and O'donnnell, A.G. (1999) Probiotics shown to change bacterial community structure in the avian gastrointestinal tract. Applied and Environmental Microbiology 65: 51345138.CrossRefGoogle ScholarPubMed
Niilo, L. (1980) Clostridium perfringens in animal disease: A review of current knowledge. Canadian Veterinary Journal 21(5): 141147.Google ScholarPubMed
Onderka, D.K., Langevin, C.C. and Hanson, J.A. (1990) Fibrosing cholehepatitis in broiler chickens induced by bile duct ligations or inoculation of Clostridium perfringens. Canadian Journal of Veterinary Research 54: 258290.Google ScholarPubMed
Ontario Ministryofagriculture, Food And Ruralaffairs (1996) Page 53 in Veterinary Laboratory Services Annual Report.Google Scholar
Panneman, H. (2001) Microbial community profiling and characterization helps the vet. World's Poultry Science Journal 17(4): 3436.Google Scholar
Panneman, H. (2002) Concept: Microbial community profiling and characterisation (MCPC) – a comparison with other methods for the diagnosis of bacterial overgrowth in the duodenum of broiler chickens. Pages E3-E7 in Proceedings from The Elanco Global Enteritis Symposium.Google Scholar
Parish, W.E. (1961) Necrotic enteritis in fowl (Gallus gallus domesticus). I. Histology of the disease and isolation of a strain of Clostridium welchii. Journal of Comparative Pathology 71: 377393.CrossRefGoogle Scholar
Pattison, M. (2002) Some clinical and pathological features of enteritis in broilers – observations on treatment in the UK. Pages C1 – C10 in Proceedings of the Poultry Enteritis ConferenceElanco Animal HealthCambridge England.Google Scholar
Prescott, J.F., Sivendra, R. and Barnum, D.A. (1978) The use of bacitracin in the prevention and treatment of experimentally-induced necrotic enteritis in the chicken. Canadian Veterinary Journal 19: 181183.Google ScholarPubMed
Porter, R.E. (1998) Bacterial enteritides of poultry. Poultry Science 77: 11591165.CrossRefGoogle ScholarPubMed
Riddell, C. and Kong, X-M. (1992) The influence of diet on necrotic enteritis in broiler chickens. Avian Diseases 36: 499503.CrossRefGoogle ScholarPubMed
Roura, E., Homedes, J. and Klasing, K.C. (1992) Prevention of immunologic stress contributes to the growth-permitting ability of dietary antibiotics in chicks. Journal of Nutrition 122: 23832390.CrossRefGoogle Scholar
Roussel, A.J. (1994) Intestinal motility. Compendium of Continuing Education for the Practicing Veterinarian 16: 14331443.Google Scholar
Rubinstein, E., Mark, Z., Haspel, J., Ben-Ari, G., Dreznik, Z., Mirelman, D. and Tadmor, A. (1985) Antibacterial activity of the pancreatic fluid. Gastroenterology 88: 927932.CrossRefGoogle ScholarPubMed
Salanitro, J.P., Blake, I.G., Muirhead, P.A., Maglio, M. and Goodman, J.R. (1978) Bacteria isolated from the duodenum, ileum and cecum of young chicks. Applied and Environmental Microbiology 35: 782–90.CrossRefGoogle ScholarPubMed
Sasaki, J., Goryo, M., Okoshi, N., Furukawa, H., Honda, J. and Okada, K. (2000) Cholangiohepatitis in broiler chickens in Japan: histopathological, immunohistochemical and microbiological studies of spontaneous disease. Acta Veterinaria Hungarica 48(1): 5967.CrossRefGoogle ScholarPubMed
Schippers, E., Willis, S., Ruckdeschel, G. and Schumpelick, V. (1996) Small intestinal myoelectrical activity and bacterial flora after Roux-en Yreconstruction. British Journal of Surgery 83: 12711275.Google Scholar
Schoorel, E.P., Giesberts, M.A., Blom, W. and Van Gelderen, H.H. (1980) D-Lactic acidosis in a boy with short bowel syndrome. Archives of Disease in Childhood 55(10): 810812.CrossRefGoogle 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: 269287.CrossRefGoogle ScholarPubMed
Sidorchuk, I.I. and Bondarenko, V.M. (1984) Selection of a biologically active mutant of Propionibacterium shermanii and the possibility of its use in complex therapy of enteral dysbacteriosis. Journal of Hygiene, Epidemiology, Microbiology and Immunology 28(3): 331338.Google ScholarPubMed
Simpson, K.W., Batt, R.M., Jones, D. and Morton, D.B. (1990) Effects of exocrine pancreatic insufficiency and replacement therapy on the bacterial flora of the duodenum in dogs. American Journal of Veterinary Research 59: 203206.CrossRefGoogle Scholar
Stutz, M.W., Johnson, S.L. and Judith, F.R. (1983) Effects of diet, bacitracin, and body weight restrictions on the intestine of broiler chicks. Poultry Science 62: 16261632.CrossRefGoogle ScholarPubMed
Stutz, M.W. and Lawton, G.C. (1984) Effects of diet and antimicrobials on growth, feed efficiency, intestinal Clostridium perfringens, and ideal weight of broiler chicks. Poultry Science 63: 20362042.CrossRefGoogle Scholar
Toskes, P.P., Giannella, R.A., Jervis, H.R., Rout, W.R. and Takeuchi, A. (1975) Small intestinal mucosal injury in the experimental blind loop syndrome; light and electron-microscopic and histochemical studies. Gastroenterology 68: 11931203.CrossRefGoogle ScholarPubMed
Truscott, R.B. and Al-Sheikhly, F. (1977) Reproduction and treatment of necrotic enteritis in broilers. American Journal of Veterinary Research 38: 857861.Google ScholarPubMed
Tsai, S.S. and Tung, M.C. (1981) An outbreak of necrotic enteritis in broiler chickens. Journal of the Chinese Society for Veterinary Science 7: 1317.Google Scholar
Utili, R., Abernathy, C.O. and Zimmerman, H. (1976) Cholestatic effects of Escherichia coli endotoxin on the isolated perfused rat liver. Gastroenterology 70: 248253.CrossRefGoogle ScholarPubMed
Visek, W.J. (1978) The mode of growth promotion by antibiotics. Journal of Animal Science 46: 14471469.CrossRefGoogle Scholar
Wahl, S.M., Hunt, D.A., Allen, J.B., Wilder, R.L., Paglia, L. and Hand, A.R. (1986) Bacterial cell wall induced heptic granulomas. Journal of Experimental Medicine 163: 884902.CrossRefGoogle Scholar
Watkins, K.L., Shryock, T.R., Dearth, R.N. and Saif, Y.M. (1997) In vitro antimicrobial susceptibility of Clostridium perfringens from commercial turkey and broiler chicken origin. Veterinary Microbiology 54: 195200.CrossRefGoogle ScholarPubMed
Wicker, D.L., Isgrigg, W.N. and Trammell, J.H. (1977) The control and prevention of necrotic enteritis in broilers with zinc bacitracin. Poultry Science 56: 12291231.CrossRefGoogle ScholarPubMed
Wilson, J., Spika, J., Clarke, R., Mcewen, S., Johnson, R., Rahn, K., Renwick, S., Karmali, M., Lior, H., Alves, D., Gyles, C. and Sandhu, K. (1996) Verocytotoxigenic Escherichia coli infection in dairy farm families. Journal of Infectious Diseases 174(5): 10211027.CrossRefGoogle Scholar
Zhu, X.Y., Zhong, T., Pandya, Y. and Joerger, R.D. (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Applied and Environmental Microbiology 68: 124137.CrossRefGoogle ScholarPubMed