Progress and problems in vaccination against necrotic enteritis in broiler chickens

Necrotic enteritis in broilers is caused by Clostridium perfringens type A strains that produce the NetB toxin. Necrotic enteritis is one of the gastrointestinal diseases in poultry that has gained worldwide importance during the last decade due to efforts to improve broiler performance. Prevention strategies include avoiding predisposing factors, such as coccidiosis, and in-feed supplementation with a variety of feed additives. However, vaccination with modified toxin or other secreted immunogenic proteins seems a logical preventive tool for protection against a toxin-producing bacterium. Formalin-inactivated crude supernatant has been used initially for vaccination. Several studies have been carried out recently to identify the most important immunogenic and protective proteins that can be used for vaccination. These include the NetB toxin, as well as a number of other proteins. There is evidence that immunization with single proteins is not protective against severe challenge and that combinations of different antigens are needed. Most published studies have used multiple dosage vaccination regimens that are not relevant for practical use in the broiler industry. Single vaccination regimens for 1-day-old chicks appear to be non-protective. This review describes the history of vaccination strategies against necrotic enteritis in broilers and gives an update on future vaccination strategies that are applicable in the field. These may include breeder hen vaccination, in ovo vaccination and live attenuated vectors to be used in feed or in drinking water.

[1]  Robert J. Moore,et al.  Maternal immunization with vaccines containing recombinant NetB toxin partially protects progeny chickens from necrotic enteritis , 2013, Veterinary Research.

[2]  R. Titball,et al.  Protection against avian necrotic enteritis after immunisation with NetB genetic or formaldehyde toxoids☆ , 2013, Vaccine.

[3]  Robert J. Moore,et al.  Vaccination with recombinant NetB toxin partially protects broiler chickens from necrotic enteritis , 2013, Veterinary Research.

[4]  F. Haesebrouck,et al.  Day-of-hatch vaccination is not protective against necrotic enteritis in broiler chickens , 2013, Avian pathology : journal of the W.V.P.A.

[5]  Robert J. Moore,et al.  Structural and Functional Analysis of the Pore-Forming Toxin NetB from Clostridium perfringens , 2013, mBio.

[6]  J. Prescott,et al.  Identification of Accessory Genome Regions in Poultry Clostridium perfringens Isolates Carrying the netB Plasmid , 2013, Journal of bacteriology.

[7]  Shixia Wang,et al.  Protective antibody responses against Clostridium difficile elicited by a DNA vaccine expressing the enzymatic domain of toxin B , 2013, Human vaccines & immunotherapeutics.

[8]  D. Moss,et al.  Molecular Architecture and Functional Analysis of NetB, a Pore-forming Toxin from Clostridium perfringens* , 2012, The Journal of Biological Chemistry.

[9]  J. Prescott,et al.  The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: a critical review , 2012, Veterinary Research.

[10]  Y. Hong,et al.  Vaccination with Clostridium perfringens recombinant proteins in combination with Montanide™ ISA 71 VG adjuvant increases protection against experimental necrotic enteritis in commercial broiler chickens. , 2012, Vaccine.

[11]  R. Rappuoli,et al.  Recombinant bacterial vaccines. , 2012, Current opinion in immunology.

[12]  D. Missiakas,et al.  Protein secretion and surface display in Gram-positive bacteria , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  C. Jakab,et al.  Efficacy of protected sodium butyrate, a protected blend of essential oils, their combination, and Bacillus amyloliquefaciens spore suspension against artificially induced necrotic enteritis in broilers. , 2012, Poultry science.

[14]  H. Lillehoj,et al.  Clostridium perfringens &agr;-Toxin and NetB Toxin Antibodies and Their Possible Role in Protection Against Necrotic Enteritis and Gangrenous Dermatitis in Broiler Chickens , 2012, Avian diseases.

[15]  L. McMullen,et al.  Hatching egg and newly hatched chick yolk sac total IgY content at 3 broiler breeder flock ages. , 2012, Poultry science.

[16]  S. Fathalla,et al.  Clinicopathological and immunological studies on toxoids vaccine as a successful alternative in controlling clostridial infection in broilers. , 2011, Anaerobe.

[17]  S. Plotkin,et al.  The development of vaccines: how the past led to the future , 2011, Nature Reviews Microbiology.

[18]  F. Levenez,et al.  Effects of stocking density on the growth performance and digestive microbiota of broiler chickens. , 2011, Poultry science.

[19]  Steven Black,et al.  Vaccine discovery and translation of new vaccine technology , 2011, The Lancet.

[20]  R. Hughes,et al.  Identification and Characterization of Potential Performance-Related Gut Microbiotas in Broiler Chickens across Various Feeding Trials , 2011, Applied and Environmental Microbiology.

[21]  J. Dewulf,et al.  Morphometric evaluation of “dysbacteriosis” in broilers , 2011, Avian pathology : journal of the W.V.P.A.

[22]  Yun-zhou Yu,et al.  Enhancement of the immunogenicity of DNA replicon vaccine of Clostridium botulinum neurotoxin serotype A by GM-CSF gene adjuvant , 2011, Immunopharmacology and immunotoxicology.

[23]  M. Francis,et al.  Safety and efficacy of a maternal vaccine for the passive protection of broiler chicks against necrotic enteritis , 2010, Avian pathology : journal of the W.V.P.A.

[24]  A. Cazemier,et al.  Efficacy of a lactylate on production performance and intestinal health of broilers during a subclinical Clostridium perfringens infection. , 2010, Poultry science.

[25]  J. Prescott,et al.  Assessment of 2 Salmonella enterica serovar Typhimurium-based vaccines against necrotic enteritis in reducing colonization of chickens by Salmonella serovars of different serogroups. , 2010, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[26]  F. Haesebrouck,et al.  Variable protection after vaccination of broiler chickens against necrotic enteritis using supernatants of different Clostridium perfringens strains. , 2010, Vaccine.

[27]  A. Batal,et al.  Evaluation of the bacterial community and intestinal development of different genetic lines of chickens. , 2010, Poultry science.

[28]  R. Davies,et al.  Effect of delivery method on the efficacy of Salmonella vaccination in chickens , 2010, Veterinary Record.

[29]  Robert J. Moore,et al.  NetB, a Pore-Forming Toxin from Necrotic Enteritis Strains of Clostridium perfringens , 2010, Toxins.

[30]  J. Dewulf,et al.  Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils , 2010, Avian pathology : journal of the W.V.P.A.

[31]  F. Haesebrouck,et al.  The effect of commonly used anticoccidials and antibiotics in a subclinical necrotic enteritis model , 2010, Avian pathology : journal of the W.V.P.A.

[32]  J. Prescott,et al.  A Live Oral Recombinant Salmonella enterica Serovar Typhimurium Vaccine Expressing Clostridium perfringens Antigens Confers Protection against Necrotic Enteritis in Broiler Chickens , 2009, Clinical and Vaccine Immunology.

[33]  Robert J. Moore,et al.  Association between avian necrotic enteritis and Clostridium perfringens strains expressing NetB toxin , 2009, Veterinary research.

[34]  J. Prescott,et al.  Immunization of Broiler Chickens Against Clostridium perfringens–Induced Necrotic Enteritis Using Purified Recombinant Immunogenic Proteins , 2009 .

[35]  D. Ho,et al.  A DNA vaccine targeting the receptor-binding domain of Clostridium difficile toxin A. , 2009, Vaccine.

[36]  R. Titball,et al.  Recombinant Bacillus subtilis Expressing the Clostridium perfringens Alpha Toxoid Is a Candidate Orally Delivered Vaccine against Necrotic Enteritis , 2008, Infection and Immunity.

[37]  J. Prescott,et al.  Oral immunization of broiler chickens against necrotic enteritis with an attenuated Salmonella vaccine vector expressing Clostridium perfringens antigens. , 2008, Vaccine.

[38]  R. Mackie,et al.  Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. , 2008, Veterinary immunology and immunopathology.

[39]  R. Curtiss,et al.  Recombinant Attenuated Salmonella enterica Serovar Typhimurium Expressing the Carboxy-Terminal Domain of Alpha Toxin from Clostridium perfringens Induces Protective Responses against Necrotic Enteritis in Chickens , 2008, Clinical and Vaccine Immunology.

[40]  Robert J. Moore,et al.  NetB, a New Toxin That Is Associated with Avian Necrotic Enteritis Caused by Clostridium perfringens , 2008, PLoS pathogens.

[41]  J. Dewulf,et al.  Quantification of gut lesions in a subclinical necrotic enteritis model , 2007, Avian pathology : journal of the W.V.P.A.

[42]  J. Prescott,et al.  Immunization of Broiler Chickens against Clostridium perfringens-Induced Necrotic Enteritis , 2007, Clinical and Vaccine Immunology.

[43]  K. Morgan,et al.  Prevalence and associated risk factors of necrotic enteritis on broiler farms in the United Kingdom; a cross-sectional survey , 2007, Avian pathology : journal of the W.V.P.A.

[44]  J. Prescott,et al.  Clostridium perfringens Antigens Recognized by Broiler Chickens Immune to Necrotic Enteritis , 2006, Clinical and Vaccine Immunology.

[45]  J. Prescott,et al.  Live attenuated vaccine-based control of necrotic enteritis of broiler chickens. , 2006, Veterinary microbiology.

[46]  G. Dietrich,et al.  Rational design of Salmonella-based vaccination strategies. , 2006, Methods.

[47]  R. Williams.  Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity , 2005, Avian pathology : journal of the W.V.P.A.

[48]  J. Lowenthal,et al.  Cytokines as adjuvants for avian vaccines , 2004, Immunology and cell biology.

[49]  L. Marraffini,et al.  Protein sorting to the cell wall envelope of Gram-positive bacteria. , 2004, Biochimica et biophysica acta.

[50]  D. Stevens,et al.  Immunization with the C-Domain of alpha -Toxin prevents lethal infection, localizes tissue injury, and promotes host response to challenge with Clostridium perfringens. , 2004, The Journal of infectious diseases.

[51]  J. Wells,et al.  Mucosal and Cellular Immune Responses Elicited by Recombinant Lactococcus lactis Strains Expressing Tetanus Toxin Fragment C , 2004, Infection and Immunity.

[52]  C. Greko,et al.  Antimicrobial susceptibility of Swedish, Norwegian and Danish isolates of Clostridium perfringens from poultry, and distribution of tetracycline resistance genes. , 2004, Veterinary microbiology.

[53]  E. Skjerve,et al.  Maternal vaccination against subclinical necrotic enteritis in broilers , 2004, Avian pathology : journal of the W.V.P.A.

[54]  F. Haesebrouck,et al.  Susceptibility of Clostridium perfringens strains from broiler chickens to antibiotics and anticoccidials , 2004, Avian pathology : journal of the W.V.P.A.

[55]  G. B. Havenstein,et al.  Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. , 2003, Poultry science.

[56]  A. Løvland,et al.  Diagnosing Clostridium perfringens-associated necrotic enteritis in broiler flocks by an immunoglobulin G anti-alpha-toxin enzyme-linked immunosorbent assay , 2003, Avian pathology : journal of the W.V.P.A.

[57]  J. Comerford,et al.  Effects of Direct-Fed Microbials on Growth, Health, and Blood Parameters of Young Holstein Calves , 2003 .

[58]  I. M. Belyakov,et al.  Strategies for designing and optimizing new generation vaccines , 2001, Nature Reviews Immunology.

[59]  J. Jarp,et al.  A field study of naturally occurring specific antibodies against Clostridium perfringens alpha toxin in Norwegian broiler flocks. , 2001, Avian diseases.

[60]  R. Gildersleeve,et al.  In ovo vaccination technology. , 1999, Advances in veterinary medicine.

[61]  J. Mast,et al.  Development of immunocompetence of broiler chickens. , 1999, Veterinary immunology and immunopathology.

[62]  D. Moss,et al.  Structure of the key toxin in gas gangrene , 1998, Nature Structural &Molecular Biology.

[63]  R. Ulrich,et al.  Are DNA-based vaccines useful for protection against secreted bacterial toxins? Tetanus toxin test case. , 1998, Vaccine.

[64]  J. Wells,et al.  Oral vaccination of mice against tetanus with recombinant Lactococcus lactis , 1997, Nature Biotechnology.

[65]  H. Hunt,et al.  Poultry vaccines of the future. , 1994, Poultry science.

[66]  O. Fossum,et al.  Factors Affecting the Incidence of Necrotic Enteritis, Caecal Carriage of Clostridium perfringens and Bird Performance in Broiler Chicks , 1992, Acta Veterinaria Scandinavica.

[67]  C. Riddell,et al.  The influence of diet on necrotic enteritis in broiler chickens. , 1992, Avian diseases.

[68]  J. Chiba,et al.  Monoclonal antibodies against alpha toxin of Clostridium perfringens. , 1989, FEMS Microbiology Letters.

[69]  F. N. Reece,et al.  Influence of a wheat diet on mortality of broiler chickens associated with necrotic enteritis. , 1987, Poultry science.

[70]  M. Hensel,et al.  Salmonella enterica as a vaccine carrier. , 2012, Future microbiology.

[71]  F. Haesebrouck,et al.  Variable protection after vaccination of broiler chickens against 6 necrotic enteritis using supernatants of different Clostridium perfringens , 2010 .

[72]  R. Titball.  Clostridium perfringens vaccines. , 2009, Vaccine.

[73]  J. Songer,et al.  Immunization with recombinant alpha toxin partially protects broiler chicks against experimental challenge with Clostridium perfringens. , 2009, Veterinary microbiology.

[74]  Robert J. Moore,et al.  Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. , 2009, Trends in microbiology.

[75]  B. Lupiani,et al.  Practical aspects of poultry vaccination , 2008 .

[76]  E. Skjerve,et al.  Reduced incidence of Clostridium perfringens-associated lesions and improved performance in broiler chickens treated with normal intestinal bacteria from adult fowl. , 2001, Avian diseases.

[77]  J. M. Sharma,et al.  Introduction to poultry vaccines and immunity. , 1999, Advances in veterinary medicine.

[78]  J. W. Deaton,et al.  The effect of added complex carbohydrates or added dietary fiber on necrotic enteritis lesions in broiler chickens. , 1997, Poultry science.

[79]  F. Bonnel,et al.  [Necrotic enteritis]. , 1973, Annales de chirurgie.

[80]  W. I. Muira,et al.  Immunity , vaccination and the avian intestinal tract , 2022 .