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Non-antibiotic strategies for the control of necrotic enteritis in poultry

Published online by Cambridge University Press:  13 November 2014

K. MAHMOOD ,
S.U. RAHMAN ,
I. HUSSAIN ,
R.Z. ABBAS ,
T. KHALIQ ,
J. ARIF  and
F. MAHMOOD
K. MAHMOOD*
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
S.U. RAHMAN
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
I. HUSSAIN
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
R.Z. ABBAS
Affiliation:
Department of Parasitology, University of Agriculture, Faisalabad, Pakistan
T. KHALIQ
Affiliation:
Department of Physiology and Pharmacology, University of Agriculture, Faisalabad, Pakistan
J. ARIF
Affiliation:
Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan
F. MAHMOOD
Affiliation:
Department of Pathology, Faculty of Veterinary science, University of Agriculture, Faisalabad, Pakistan
*
Corresponding author: kmvoh@yahoo.com
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Abstract

Necrotic enteritis (NE) caused by Clostridium spp. is an economically significant bacterial disease of poultry worldwide. Traditionally the disease has been prevented through feed supplementation with antibiotics sub-therapeutically as antimicrobial growth promoters (AGPs). However this practice has led to the emergence of resistant pathogenic microbes and drug residues, potentially threatening animal and public health. Therefore the marketing and incorporation of AGPs into poultry feed has been banned in Europe which has exacerbated the incidence of NE, bringing about huge economic losses to poultry farmers. Poultry researchers, exporters and consumers have emphasised AGP-free poultry rearing and have been searching for non-antibiotic and cost effective alternatives to control NE. Strategies suggested include vaccination, coccidiosis control, probiotics, competitive exclusion products, prebiotics, egg yolk immunoglobulins, bacteriophages (or phage gene products), organic acids, feed enzymes, plants and plants extracts/essential oils and nutritional changes.

There are many predisposing as well as virulence factors for NE induction and pathogenesis and more are expected to be discovered in the future. The ambiguous pathogenesis trend of the disease is still hindering the development of a potent active vaccine against NE. The choice of a single and fully effective approach is difficult. However, probiotics and specific egg yolk immunoglobulins (IgYs) alone or in combination could serve as promising strategies for controlling NE in broilers in the absence of AGPs.

Keywords

Necrotic enteritisClostridium perfringensprobioticsegg yolk immunoglobulinsbacteriophages
Type
Review Article
Information
World's Poultry Science Journal , Volume 70 , Issue 4 , December 2014 , pp. 865 - 879
Copyright
Copyright © World's Poultry Science Association 2014 

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References

ABBAS, R.Z., IQBAL, Z., BLAKE, D., KHAN, M.N. and SALEEMI, M.K. (2011) Anticoccidial drug resistance in fowl coccidia: the state of play revisited. World's Poultry Science Journal 67: 337-350.Google Scholar
ABBAS, R.Z., CLOWELL, D. and GILLEARD, J. (2012a) Botanicals: an alternative approach for the control avian coccidiosis. World's Poultry Science Journal 68: 203-215.Google Scholar
ABBAS, R.Z., IQBAL, Z., KHAN, A., SINDHU, Z.U.D., KHAN, J.A., KHAN, M.N. and RAZA, A. (2012b) Options for integrated strategies for the control of avian coccidiosis. International Journal of Agriculture and Biology 14: 1014-1020.Google Scholar
ABILGAARD, L., SONDERGAARD, T.T., ENBERG, 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 doi:10.1016/j.vetmic.12.036.Google Scholar
ADAMS, C.A. (2004) Nutrition in poultry production: focus on bioactive feed ingredients. Nutrition Abstracts Review Series B 74: 1N-12N.Google Scholar
ADIJIRI-AWERE, A. and VAN LUNEN, T.A. (2005) Subtherapeutic use of antibiotics in pork production: Risks and alternatives. Canadian Journal of Animal Science 85: 117-130.Google Scholar
AL-KASSIE, G.A.M. (2009) Influence of two plant extracts derived from thyme and cinnamon on broiler performance. Pakistan Veterinary Journal 29: 169-173.Google Scholar
ANNET, 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 31: 598-601.CrossRefGoogle Scholar
APAJALAHTI, J.H. (2004) Structure and dietary modulation of intestinal microbial communities, in: Second Mid-Atlantic Nutrition Conference, pp. 69-76 (University of Maryland, College Park, Timonium, MD).Google Scholar
BIERNASIAK, J., SILIZEWSKA, K., LIBUDZISZ, Z. and SMULIKOWSKA, S. (2007) Effect of dietary probiotic containing Lactobacillus bacteria, yeast and yucca extract on the performance and faecal microflora of broiler chickens. Polish Journal of Food and Nutrition Science 57: 19-25.Google Scholar
BJERRUM, L., PEDERSEN, A.B. and ENBERG, R.M. (2005) The influence of whole wheat feeding on Salmonella infection and gut flora composition in broilers. Avian Diseases 49: 9-15.Google Scholar
BOOSTANI, A., MAHMOODIAN FARD, H.R., ASHAYERIZADEH, A. and AMINAFSHAR, M. (2013) Growth performance, carcass yield and intestinal microflora populations of broilers fed diets containing thepax and yogurt. Brazilian Journal of Poultry Science ISSN 1516-635X Jan-Mar 2013/v.15/n.1/1-6.Google Scholar
BOZKURT, M., KÜÇÜKYILMAZ, K., CATH, A.U. and ÇINAR, M. (2009) The effect of single or combined dietary supplementation of prebiotics, organic acid and probiotics on performance and slaughter characteristics of broilers. The South African Journal of Animal Science 39 (3) at: http: //www.sasas.co.za/sajas.asp (online).Google Scholar
BRENES, A. and ROURA, E. (2010) Essential oils in poultry nutrition: Main effects and modes of action. Animal Feed Science and Technology 158: 1-14.Google Scholar
BRYNESTAD, S. and GRANUM, P.E. (2002) Clostridium perfringens and food-borne infections. International Journal of Food Microbiology 74: 195-202.Google Scholar
CARDOZO, M.V., SCHOCKEN-ITURRINO, R.P., BERALDO-MASSOLI, M.C., CAVANI, R., CASAGRANDE, M.F., BORINI, L., BORGES, C.A. and BERALDO, L.G. (2012) Pathogens in meal and the use of Salmex® in the elimination of Clostridium perfringens. African Journal of Microbiology Research 6: 3727-3731.Google Scholar
CASTANON, J.I. (2007) History of the use of antibiotic growth promoters in European poultry feeds. Poultry Science 86: 2466-2471.Google Scholar
COOPER, K.K., TRINH, H.T. and SONGER, J.G. (2009) Immunisation with recombinant alpha toxin partially protects broiler chicks against experimental challenge with Clostridium perfringens. Veterinary Microbiology 133: 92-97.Google Scholar
DE SMET, S. and VERLEYEN, T. (2010) Prevent the proliferation of clostridial enteritis. World Poultry (Necrotic Enteritis Special), pp: 8-9.Google Scholar
DIARRA, M.S., SILVERSIDES, F.G., DIARRASSOUBA, F., PRITCHARD, J., MASSON, L., BROUSSEAU, R., BONNET, C., DELAQUIS, P., BACH, S., SKURA, B.J. and TOPP, E. (2007) Impact of feed supplementation with antimicrobial agents on growth performance of broiler chickens, Clostridium perfringens and Enterococcus counts and antibiotic resistance phenotypes and distribution of antimicrobial resistance determinants in Escherichia coli isolates. Applied Environmental Microbiology 73: 6566-6576.Google Scholar
DUNCAN, S.H., LOUIS, P. and FLINT, H.J. (2004) Lactate-utilizing bacteria, isolated from human feces that produce butyrate as a major fermentation product. Applied Environmental Microbiology 70: 5810-5817.Google Scholar
ENBERG, R.M., GREVSEN, K., IVARSEN, E., FRETTÉ, X., CHRISTENSEN, L.P., HØJBERG, O., JENSEN, B.B. and CANIBE, N. (2012) The effect of Artemisia annua on broiler performance, on intestinal microbiota and on the course of a Clostridium perfringens infection applying a necrotic enteritis disease model. Avian Pathology 41: 369-376.Google Scholar
ENBERG, R.M., HEDEMANN, M.S. and JENSEN, B.B. (2002) The influence of grinding and pelleting of feed on the microbial composition and activity in the digestive tract of broiler chickens. British Poultry Science 43: 569-579.Google Scholar
FERNANDEZ, F., HINTON, M. and VAN GLIS, B. (2002) Dietary mannan-oligosaccharides and their effect on chicken caecal microflora in relation to Salmonella enteritidis colonisation. Avian Pathology 31: 49-58.Google Scholar
FERNANDEZ DA COSTA, S.P., MOT, D., BOKORI-BROWN, M., SAVVA, C.G., BASAK, A.K., VAN IMMERSEEL, F. and TITBALL, R.W. (2013) Protection against avian necrotic enteritis after immunisation with netB genetic or formaldehyde toxoid. Vaccine 31: 4003-4008.Google Scholar
GAD, W., HAUK, R., KRÜGER, M. and HAFEZ, H.M. (2011) Prevalence of Clostridium perfringens in commercial turkey and layer flocks . Archives für Geflügelkunde 75: 74-79.Google Scholar
GEIER, M.S., MIKKELSEN, L.I., TOROK, V.A., ALLISON, G.E., OLNOOD, C.G., BOULIANNE, M., HUGHES, R.J. and CHOCT, M. (2010) Comparison of alternatives to in-feed antimicrobials for the prevention of clinical necrotic enteritis. Journal of Applied Microbiology 109: 1329-1338.Google Scholar
GERVASI, T., LO CURTO, R., NARBAD, A. and MAYER, M.J. (2013a) Complete genome sequence of PhiCP51, A temperate bacteriophage of Clostridium perfringens. Archives of Virology doi: 10.1007/S00 705-013-1647-1.Google Scholar
GERVASI, T., HORN, N. and WEGMANN, U. (2013b) Expression and delivery of an endolysin to combat Clostridium perfringens. Applied Microbiology and Biotechnology, doi: 10.1007/S00253-103-5128-y.Google Scholar
GHOLAMIANDEHKORDI, A.R., TIMBERMONT, L., LANCKRIET, A., VAN DEN BROECK, W., PEDERSON, K., J. DEWULF, J., PASMANS, F., HAESEBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2007) Quantification of gut lesions in a subclinical necrotic enteritis model. Avian Pathology 36: 375-382.Google Scholar
HAMAL, K.R., BURGESS, S.C., PEVZNER, I.Y. and ERF, G.F. (2006) Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poultry Science 85: 1364-1372.Google Scholar
HUYGHEBAERT, G., DUCATELLE, R. and VAN IMMERSEEL, F.P. (2011) An update on alternatives to antimicrobial growth promoters for broilers. Veterinary Journal 187: 182-188. doi: 10.1016/j.tvjl.2010.03.003.Google Scholar
ISLAM, M.N., RASHID, S.M.H., JULI, M.S.B., HOQUE, M.F. and AKHTER, M.R. (2009) Necrotic enteritis in chickens: Pathological, bacteriological and therapeutical investigation. International Journal of Sustainable Crop Production 4: 1-8.Google Scholar
IVARSEN, E., FRETTÉ, X.E., CHRISTENSEN, K.B., ENBERG, R.M., KJAER, A., JENSEN, M., GREVSEN, K. and CHRISTENSEN, L.P. (2010) Evaluation of the efficiency of essential oil compounds from A. annua as an antimicrobial against Clostridium perfringens in poultry. Abstracts book of 6th Conference on medicinal and aromatic plants of Southeast European countries (CMAPSEEC); Antalya, Turkey, Phcog. Mag. 6 (Suppl.), pp. 126.Google Scholar
JIA, W., SLOMINSKY, B.A., BRUCE, H.L., BLANK, G., CROW, G. and JONES, O. (2009) Effect of diet type and enzyme addition on growth performance and gut health of broiler chickens during subclinical Clostridium perfringens challenge. Poultry Science 88: 132-140.Google Scholar
KARLSSON, M., KOLLBERG, H. and LARSSON, A. (2004) Chicken IgY: utilizing the evolutionary advantage. World's Poultry Science Journal 60: 341-348.Google Scholar
KASSAIFY, Z.G. and MINE, Y. (2004) Effect of food protein supplements on Salmonella enteritidis infection and prevention in laying hens. Poultry Science 83: 753-760.Google Scholar
KEYBURN, A.L., SHEEDY, S.A., FORD, M.E., WILLIAMSON, M.M., AWAD, M.M., ROOD, J.I. and MOORE, R.J. (2006) Alpha-toxin of Clostridium perfringens is not an essential virulence factor in necrotic enteritis in chickens. Infection and Immunity 74: 6496-6500.Google Scholar
KEYBURN, A.L., YAN, X.X., BANNUM, T.L., VAN IMMERSEEL, F., ROOD, J.I. and MOORE, R.J. (2010) Association between avian necrotic enteritis and Clostridium perfringens strains expressing netB toxin. Veterinary Research 41: 21.Google Scholar
KNAP, I., LUND, B.T. and AUGUSTSSON, E.U. (2010) Prevents necrotic enteritis by use of Bacillus licheniformis (GalliPro Tect) and improves performance in broiler chickens. Proceedings of International poultry Scientific Forum 2010. Atlanta, US. M66.Google Scholar
KULKARNI, R.R., PARREIRA, V.R., SHARIF, S. and PRESCOTT, J.F. (2006) Clostridium perfringens antigens recognised by broiler chickens immune to necrotic enteritis. Clinical and Vaccinal Immunology 13: 1358-1362.Google Scholar
KULKARNI, R.R., PARREIRA, V.R., JIANG, Y.F. and PRESCOTT, J.F. (2010) A live oral recombinant Salmonella enterica serovar Typhimuricum vaccine expressing Clostridium perfringens antigens confers protection against necrotic enteritis in broiler chickens. Clinical and Vaccinal Immunology 17: 205-214.Google Scholar
LANCKRIET, A., TIMBERMONT, L., EECKHAUT, V., HAESEBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2010) Variable protection after vaccination of broiler chickens against necrotic enteritis using supernatants of different Clostridium perfringens strains. Vaccine 28: 5920-5923.Google Scholar
LEE, S.H., LILLEHOJ, H.S., PARK, D.W., HONG, Y.H. and KIN, J.J. (2007b) Effects of Pediococcus-based probiotic (MitoMax®) on coccidiosis in broiler chickens. Comparative Immunology and Microbiology of Infectious Diseases 30: 261.Google Scholar
LEE, S.H., LILLEHOJ, H.S., DALLOUL, R.A., PARK, D.W., HONG, Y.H. and LIN, J.J. (2007a) Influence of Pediococcus-based probiotic on coccidiosis in broilers chickens. Poultry Science 86: 63-66.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
MACKLIN, K.S. and KREHLING, J.T. (2010) The effect of essential oils on inhibiting growth of Clostridium perfringens. Proceedings of International Poultry Scientific Forum 2010, Atlanta, US. P169.Google Scholar
MASOOD, S., ABBAS, R.Z., IQBAL, Z., MANSOOR, M.K., SINDHU, Z.U.D., ZIA, M.A. and KHAN, J.A. (2013) Role of natural antioxidants for the control of coccidiosis in poultry. Pakistan Veterinary Journal 33: 401-407.Google Scholar
MCREYNOLDS, J., WANECK, C., BYRD, J., GENOVESE, K., DUKE, S. and NISBET, D. (2009) Efficacy of multistrain direct-fed microbial and phytogenetic products in reducing necrotic enteritis in commercial broilers. Poultry Science 88: 2075-2080.CrossRefGoogle ScholarPubMed
MEAD, G.C. (2000) Prospects for ‘competitive exclusion’ treatment to control salmonellas and other food-borne pathogens in poultry. Veterinary Journal 159: 111-123.Google Scholar
MILLER, R.W., SKINNER, J., SULAKVELIDZE, A., MATHIS, G.F. and HOFACRE, C.L. (2010) Bacteriophage therapy for control of necrotic enteritis of broiler chickens experimentally infected with Clostridium perfringens. Avian Diseases 54: 33-40.Google Scholar
MOT, D., TIMBERMONT, L., DELEZIE, E., HAESEBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2013) Day-of-hatch vaccination is not protective against necrotic enteritis in broiler chickens. Avian Pathology 42: 179-184.Google Scholar
NIBA, A.T., KOUCHIKA, H., KUDI, A.C., BEAL, J.D. and BROOKS, P.H. (2013) Effect of microorganisms and particle size on fermentation of sorghum and maize for poultry feed. African Journal of Biotechnology 12: 4147-4157.Google Scholar
PANDA, K., RAO, S.V.R. and RAJU, M.V.L.N. (2006) Natural growth promoters have potential in poultry feeding systems. Feed Technology 8: 23-26.Google Scholar
PAN, X.D., CHEN, F.Q., WU, T.K., TANG, H.G. and ZHAO, Z.Y. (2009) Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of bowel. Journal of Zhejiang University of Science 10: 258-263.Google Scholar
RADA, V., RYCHLÝ, I. and VORÍŠEK, K. (1994) Susceptibility of chicken intestinal lactobacilli to coccidiostats. Acta Veterinariya 63: 9-12.Google Scholar
RAMIREZ-FARIAS, C., SLEZK, K., FULLER, Z., DUNCAN, A., HOLTROP, G. and LOUIS, P. (2009) Effect of inulin on the human gut microbiota: Stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. British Journal of Nutrition 101: 541-550.Google Scholar
SAWIRES, Y.S. and SONGER, J.G. (2006) Clostridium perfringens: insight into virulence evolution and population structure. Anaerobe 12: 23-43.Google Scholar
SEAL, B.S. (2013) Characterisation of bacteriophages virulent for Clostridium perfringens and identification of the phage lytic enzymes as alternatives to antibiotics for potential control of the bacterium. Poultry Science 92: 526-33.Google Scholar
SHERMAN, P.M., OSSA, J.C. and JOHNSON-HENRY, K. (2009) Unravelling mechanisms of action of probiotics. Nutritional Clinical Practices 21: 10-14.Google Scholar
SHIRLEY, M.W. and LILLEHOJ, H.S. (2012) The long view: a selective review of 40 years of coccidiosis research. Avian Pathology 41: 111-121.Google Scholar
SI, W., NI, X., GONG, J., YU, H., TSAO, R., HAN, Y. and CHAMBERS, J.R. (2009) Antimicrobial activity of essential oils and structurally related synthetic food additives towards Clostridium perfringens. Journal of Applied Microbiology 106: 213-220.Google Scholar
SIMMONS, M., DONOVAN, D.M., SIRAGUSA, G.R. and SEAL, B.S. (2010) Recombinant expression of two bacteriophage proteins that lyse Clostridium perfringens and share identical sequences in the C-terminal cell wall binding domain of the molecules but are dissimilar in their N-terminal active domains. Journal of Agriculture and Food Chemistry 58: 10330-10337.Google Scholar
SIRAGUSA, G.R., HASS, G.J., MATHEWS, P.D., SMITH, R.J., BUHR, R.J., DALE, N.M. and WISE, M.G. (2008) Antimicrobial activity of lupulone against Clostridium perfringens in the chicken intestinal tract jejunum and caecum. Journal of Antimicrobial Chemotherapy 61: 853-858.Google Scholar
SMYTH, J.A. and MARTIN, T.G. (2010) Disease producing capability of netB positive isolates of C. perfringens recovered from normal chickens and a cow, and netB positive and negative isolates from chickens with necrotic enteritis. Veterinary Microbiology 146: 76-84.CrossRefGoogle Scholar
TAMILZARASAN, K.B., DINAKARAN, A.M., SELVARAJU, G. and DORARIAJAN, N. (2009) Efficacy of egg-yolk immunoglobulins (IGY) against enteric pathogens in poultry. Tamilnadu Journal of Veterinary Animal Science 5: 264-268.Google Scholar
TEIRLYNCK, E., KJERRUM, L., EEKHAUT, V., HUYGHEBAERT, G., PASMANS, F., HAESBROUCK, F., DEWULF, J., DUCATELLE, R. and VAN IMMERSEEL, F. (2009) The cereal type in feed influences gut wall morphology and intestinal immune cell infiltration in broiler chickens . British Journal of Nutrition 102: 1453-1561.Google Scholar
TEO, A.Y. and TAN, H.M. (2005) Inhibition of Clostridium perfringens by a novel strain of Bacillus subtilis isolated from the gastrointestinal tracts of healthy chickens. Applied Environmental Microbiology 71: 4185-4190.Google Scholar
THOMPSON, D.R., PARREIRA, V.R., KULKARNI, R.R. and PRESCOTT, J.F. (2006) Live attenuated vaccine-based control of necrotic enteritis of broiler chickens. Veterinary Microbiology 113: 25-34.Google Scholar
TIMBERMONT, L. (2009) A contribution to the pathogenesis and treatment of Clostridium perfringens-associated necrotic enteritis in broilers. Ph. D. Thesis, Faculty of Veterinary medicine, Ghent University.Google Scholar
TIMBERMONT, L., LANCKRIET, A., GHOLAMIANDEHKORDI, A.R., PASMANS, F., MARTEL, A., HAESBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2009b) Origin of Clostridium perfringens isolates determines the ability to induce necrotic enteritis in broilers. Comparative Immunology and Microbiology of Infectious Diseases 32: 503-512.Google Scholar
TIMBERMONT, L., LANCKRIET, A., PASMANS, F., HAESBROUCK, F., DUCATELLE, R. and VAN IMMERSEEL, F. (2009a) Intra-species growth-inhibition by Clostridium perfringens is a possible virulence trait in necrotic enteritis in broilers. Veterinary Microbiology 137: 388-391.Google Scholar
VAN DER SLUIS, W. (2010) Global threat of bacterial enteritis continues to grow. World Poultry 26: 26-29.Google Scholar
VAN IMMERSEEL, F., RUSSEL, J.B., FLYTHE, M.D., GANTOIS, I., TIMBERMONT, L., PASMANS, F., HAESEBROUCK, F. and DUCATELLE, R. (2006) The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathology 35: 182-188.Google Scholar
VAN IMMERSEEL, F., ROOD, J.I., MOORE, R.J. and TITBALL, R.W. (2009) Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends in Microbiology 17: 32-36.CrossRefGoogle ScholarPubMed
VOLOZHANTSEV, N.V., OAKLEY, B.B., MORALES, C.A., VEREVKIN, V.E., BANNOV, V.A., KRASILNIKOVA, V.M., POPOVA, A.V., ZHILENKOV, E.L., GARRISH, J.K., SCHEGG, K.M., WOOLSEY, R., QUILICI, D.R., LINE, J.E., HIETT, K.L., SIRAGUSA, G.R., SVETOCH, E.A. and SEAL, B.S. (2012) Molecular characterisation of podoviral bacteriophages virulent for Clostridium perfringens and their comparison with members of the Picovirinae. PloS ONE 7(5): e38283. Open access at: www.plosone.org (online).Google Scholar
WANG, G., ZHOU, J., ZHENG, F., LIN, G., CAO, X., GONG, X. and QIU, C. (2011) Detection of different genotypes of Clostridium perfringens in feces of healthy dairy cattle from China using real-time duplex PCR assay. Pakistan Veterinary Journal 3: 120-124.Google Scholar
WILKIE, D.C., VAN KESSEL, A.G., DUMONCEUAX, T.J. and DREW, M.D. (2006) The effect of hen-egg antibodies on Clostridium perfringens colonisation in the gastrointestinal tract of broiler chickens. Preview of Veterinary Medicine 74: 279-292.CrossRefGoogle ScholarPubMed
WU, S.B., RODGERS, N. and CHOCT, M. (2010) Optimised necrotic enteritis model producing clinical and subclinical infection of Clostridium perfringens in broiler chickens. Avian Diseases 54: 1058-1065.Google Scholar
ZEKARIAS, B., MO, H. and CURTISS III, R. (2008) Recombinant attenuated Salmonella enterica serovar Typhimuricum expressing the Carboxi-Terminal domain of alpha-toxin from Clostridium perfringens induces protective responses against necrotic enteritis in chickens. Clinical and Vaccinal Immunology 15: 805-816.Google Scholar
ZIMMER, M., VUKOS, N., SCHERER, S. and LOESSNER, M.J. (2002) The murein hydrolase of the bacteriophage ɸ3626 dual lysis system is active against all tested Clostridium perfringens strains. Applied Environmental Microbiology 68: 5311-5317.Google Scholar