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Necrotic enteritis in chickens: a review of pathogenesis, immune responses and prevention, focusing on probiotics and vaccination

Published online by Cambridge University Press:  25 January 2022

Mohammadali Alizadeh Open the ORCID record for Mohammadali Alizadeh [Opens in a new window] ,
Bahram Shojadoost ,
Nitish Boodhoo ,
Jake Astill ,
Khaled Taha-Abdelaziz ,
Douglas C. Hodgins ,
Raveendra R. Kulkarni  and
Shayan Sharif
Mohammadali Alizadeh
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada
Bahram Shojadoost
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada
Nitish Boodhoo
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada
Jake Astill
Affiliation:
Artemis Technologies Inc., Guelph, Ontario, Canada
Khaled Taha-Abdelaziz
Affiliation:
Department of Animal and Veterinary Sciences, Clemson University, Clemson, SC, 29634, USA
Douglas C. Hodgins
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada
Raveendra R. Kulkarni
Affiliation:
Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, NC, 27607, USA
Shayan Sharif*
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada
*
Author for correspondence: Shayan Sharif, Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, OntarioN1G 2W1, Canada. E-mail: [email protected]
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Abstract

Necrotic enteritis (NE), caused by Clostridium perfringens (CP), is one of the most common of poultry diseases, causing huge economic losses to the poultry industry. This review provides an overview of the pathogenesis of NE in chickens and of the interaction of CP with the host immune system. The roles of management, nutrition, probiotics, and vaccination in reducing the incidence and severity of NE in poultry flocks are also discussed.

Keywords

ChickensClostridium perfringensimmune responsenecrotic enteritispathogenesisprobioticsvaccination
Type
Review Article
Information
Animal Health Research Reviews , Volume 22 , Issue 2 , December 2021 , pp. 147 - 162
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Adhikari, P, Kiess, A, Adhikari, R and Jha, R (2020) An approach to alternative strategies to control avian coccidiosis and necrotic enteritis. Journal of Applied Poultry Research 29, 515–534.CrossRefGoogle Scholar
Akbari, MR, Haghighi, HR, Chambers, JR, Brisbin, J, Read, LR and Sharif, S (2008) Expression of antimicrobial peptides in cecal tonsils of chickens treated with probiotics and infected with Salmonella enterica serovar typhimurium. Clinical and Vaccine Immunology 15, 1689–1693.CrossRefGoogle ScholarPubMed
Aliakbarpour, HR, Chamani, M, Rahimi, G, Sadeghi, AA and Qujeq, D (2012) The Bacillus subtilis and lactic acid bacteria probiotics influences intestinal mucin gene expression, histomorphology and growth performance in broilers. Asian-Australasian Journal of Animal Sciences 25, 1285.CrossRefGoogle ScholarPubMed
Alizadeh, M, Rogiewicz, A, McMillan, E, Rodriguez-Lecompte, JC, Patterson, R and Slominski, BA (2016) Effect of yeast-derived products and distillers dried grains with solubles (DDGS) on growth performance and local innate immune response of broiler chickens challenged with Clostridium perfringens. Avian Pathology 45, 334–345.CrossRefGoogle ScholarPubMed
Alizadeh, M, Shojadoost, B, Astill, J, Taha-Abdelaziz, K, Karimi, SH, Bavananthasivam, J, Kulkarni, RR and Sharif, S (2020) Effects of in ovo inoculation of multi-strain Lactobacilli on cytokine gene expression and antibody-mediated immune responses in chickens. Frontiers in Veterinary Science 7, 105.CrossRefGoogle ScholarPubMed
Allen, PC and Fetterer, RH (2002) Recent advances in biology and immunobiology of Eimeria species and in diagnosis and control of infection with these coccidian parasites of poultry. Clinical Microbiology Reviews 15, 58–65.CrossRefGoogle Scholar
Annett-Christianson, C (2012) Effect of Wheat and Corn on the Proliferation of Clostridium perfringens Type a and the Prevalence and Importance of Clostridium perfringens in Broiler Chickens in Saskatchewan (PhD thesis). University of Saskatchewan, Saskatoon, Saskatchewan, Canada.Google Scholar
Azad, M, Kalam, A, Sarker, M and Wan, D (2018) Immunomodulatory effects of probiotics on cytokine profiles. BioMed Research International 2018. doi:10.1155/2018/8063647.CrossRefGoogle ScholarPubMed
Bai, SP, Wu, AM, Ding, XM, Lei, Y, Bai, J, Zhang, KY and Chio, JS (2013) Effects of probiotic-supplemented diets on growth performance and intestinal immune characteristics of broiler chickens. Poultry Science 92, 663–670.CrossRefGoogle ScholarPubMed
Bangoura, B, Alnassan, AA, Lendner, M, Shehata, AA, Krüger, M and Daugschies, A (2014) Efficacy of an anticoccidial live vaccine in prevention of necrotic enteritis in chickens. Experimental Parasitology 145, 125–134.CrossRefGoogle ScholarPubMed
Bearson, S, Bearson, B and Foster, JW (1997) Acid stress responses in enterobacteria. FEMS Microbiology Letters 147, 173–180.CrossRefGoogle ScholarPubMed
Ben Lagha, A, Haas, B, Gottschalk, M and Grenier, D (2017) Antimicrobial potential of bacteriocins in poultry and swine production. Veterinary Research 48, 1–12.CrossRefGoogle ScholarPubMed
Bermudez-Brito, M, Plaza-Díaz, J, Muñoz-Quezada, S, Gómez-Llorente, C and Gil, A (2012) Probiotic mechanisms of action. Annals of Nutrition and Metabolism 61, 160–174.CrossRefGoogle ScholarPubMed
Boekhorst, J, Helmer, Q, Kleerebezem, M and Siezen, RJ (2006) Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology (Reading, England) 152, 273–280.CrossRefGoogle ScholarPubMed
Brisbin, JT, Zhou, H, Gong, J, Sabour, P, Akbari, MR, Haghighi, HR, Yu, H, Clarke, A, Sarson, AJ and Sharif, S (2008) Gene expression profiling of chicken lymphoid cells after treatment with Lactobacillus acidophilus cellular components. Developmental and Comparative Immunology 32, 563–574.CrossRefGoogle ScholarPubMed
Brisbin, JT, Gong, J, Orouji, S, Esufali, J, Mallick, AI, Parvizi, P, Shewen, PE and Sharif, S (2011) Oral treatment of chickens with lactobacilli influences elicitation of immune responses. Clinical and Vaccine Immunology 18, 1447–1455.CrossRefGoogle ScholarPubMed
Brisbin, JT, Parvizi, P and Sharif, S (2012) Differential cytokine expression in T-cell subsets of chicken caecal tonsils co-cultured with three species of Lactobacillus. Beneficial Microbes 3, 205–210.CrossRefGoogle ScholarPubMed
Calefi, AS, Honda, BTB, Costola-de-Souza, C, de Siqueira, A, Namazu, LB, Quinteiro-Filho, WM, da Silva Fonseca, JG, Aloia, TPA, Piantino-Ferreira, AJ and Palermo-Neto, J (2014) Effects of long-term heat stress in an experimental model of avian necrotic enteritis. Poultry Science 93, 1344–1353.CrossRefGoogle Scholar
Caly, DL, D'Inca, R, Auclair, E and Drider, D (2015) Alternatives to antibiotics to prevent necrotic enteritis in broiler chickens: a microbiologist's perspective. Frontiers in Microbiology 6, 1336.CrossRefGoogle ScholarPubMed
Cao, L, Yang, XJ, Li, ZJ, Sun, FF, Wu, XH and Yao, JH (2012) Reduced lesions in chickens with Clostridium perfringens-induced necrotic enteritis by Lactobacillus fermentum 1.2029. Poultry Science 91, 3065–3071.CrossRefGoogle Scholar
Chelakkot, C, Ghim, J and Ryu, SH (2018) Mechanisms regulating intestinal barrier integrity and its pathological implications. Experimental & Molecular Medicine 50, 1–9.CrossRefGoogle ScholarPubMed
Chen, ML, Ge, Z, Fox, JG and Schauer, DB (2006) Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infection and Immunity 74, 6581–6589.CrossRefGoogle ScholarPubMed
Collier, CT, Hofacre, CL, Payne, AM, Anderson, DB, Kaiser, P, Mackie, RI and Gaskins, HR (2008) Coccidia-induced mucogenesis promotes the onset of necrotic enteritis by supporting Clostridium perfringens growth. Veterinary Immunology and Immunopathology 122, 104–115.CrossRefGoogle ScholarPubMed
Cooper, KK, Trinh, HT and Songer, JG (2009) Immunization with recombinant alpha toxin partially protects broiler chicks against experimental challenge with Clostridium perfringens. Veterinary Microbiology 133, 92–97.CrossRefGoogle ScholarPubMed
Cotter, PD, Ross, RP and Hill, C (2013) Bacteriocins – a viable alternative to antibiotics? Nature Reviews Microbiology 11, 95–105.CrossRefGoogle ScholarPubMed
Cuperus, T, Coorens, M, van Dijk, A and Haagsman, HP (2013) Avian host defense peptides. Developmental and Comparative Immunology 41, 352–369.CrossRefGoogle ScholarPubMed
da Costa, SPF, Mot, D, Bokori-Brown, M, Savva, CG, Basak, AK, Van Immerseel, F and Titball, RW (2013) Protection against avian necrotic enteritis after immunisation with NetB genetic or formaldehyde toxoids. Vaccine 31, 4003–4008.CrossRefGoogle Scholar
Davani, D, Pancer, Z and Ratcliffe, MJH (2014) Ligation of surface Ig by gut-derived antigen positively selects chicken bursal and peripheral B cells. Journal of Immunology 192, 3218–3227.CrossRefGoogle ScholarPubMed
Degen, WGJ, Van Zuilekom, HI, Scholtes, NC, Van Daal, N and Schijns, VEJC (2005) Potentiation of humoral immune responses to vaccine antigens by recombinant chicken IL-18 (rChIL-18). Vaccine 23, 4212–4218.CrossRefGoogle Scholar
De Geus, ED and Vervelde, L (2013) Regulation of macrophage and dendritic cell function by pathogens and through immunomodulation in the avian mucosa. Developmental and Comparative Immunology 41, 341–351.CrossRefGoogle ScholarPubMed
Dobson, A, Cotter, PD, Ross, RP and Hill, C (2012) Bacteriocin production: a probiotic trait? Applied and Environmental Microbiology 78, 1–6.CrossRefGoogle ScholarPubMed
Drew, MD, Syed, NA, Goldade, BG, Laarveld, B and Van Kessel, AG (2004) Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens. Poultry Science 83, 414–420.CrossRefGoogle ScholarPubMed
Dunlop, MW, Moss, AF, Groves, PJ, Wilkinson, SJ, Stuetz, RM and Selle, PH (2016) The multidimensional causal factors of ‘wet litter' in chicken-meat production. Science of the Total Environment 562, 766–776.CrossRefGoogle ScholarPubMed
Elwinger, K, Berndtson, E, Engström, 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.CrossRefGoogle ScholarPubMed
Emami, NK, Calik, A, White, MB, Young, M and Dalloul, RA (2019) Necrotic enteritis in broiler chickens: the role of tight junctions and mucosal immune responses in alleviating the effect of the disease. Microorganisms 7, 231.CrossRefGoogle ScholarPubMed
Fasina, YO and Lillehoj, HS (2019) Characterization of intestinal immune response to Clostridium perfringens infection in broiler chickens. Poultry Science 98, 188–198.CrossRefGoogle ScholarPubMed
Gagliardi, A, Totino, V, Cacciotti, F, Iebba, V, Neroni, B, Bonfiglio, G, Trancassini, M, Passariello, C, Pantanella, F and Schippa, S (2018) Rebuilding the gut microbiota ecosystem. International Journal of Environmental Research and Public Health 15, 1679.CrossRefGoogle ScholarPubMed
Gholamiandehkordi, AR, Timbermont, L, Lanckriet, A, Van Den Broeck, W, Pedersen, K, 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.CrossRefGoogle Scholar
Grilli, E, Messina, MR, Catelli, E, Morlacchini, M and Piva, A (2009) Pediocin A improves growth performance of broilers challenged with Clostridium perfringens. Poultry Science 88, 2152–2158.CrossRefGoogle ScholarPubMed
Gu, C, Lillehoj, HS, Sun, Z, Lee, Y, Zhao, H, Xianyu, Z, Yan, X, Wang, Y, Lin, S, Liu, L and Li, C (2019) Characterization of virulent netB + /tpeL + Clostridium perfringens strains from necrotic enteritis-affected broiler chicken farms. Avian Diseases 63, 461–467.CrossRefGoogle ScholarPubMed
Guardia, S, Konsak, B, Combes, S, Levenez, F, Cauquil, L, Guillot, J-F, Moreau-Vauzelle, C, Lessire, M, Juin, H and Gabriel, I (2011) Effects of stocking density on the growth performance and digestive microbiota of broiler chickens. Poultry Science 90, 1878–1889.CrossRefGoogle ScholarPubMed
Guo, S, Li, C, Liu, D and Guo, Y (2015) Inflammatory responses to a Clostridium perfringens type A strain and α-toxin in primary intestinal epithelial cells of chicken embryos. Avian Pathology 44, 81–91.CrossRefGoogle ScholarPubMed
Guo, S, Liu, D, Zhang, B, Li, Z, Li, Y, Ding, B and Guo, Y (2017) Two Lactobacillus species inhibit the growth and α-toxin production of Clostridium perfringens and induced proinflammatory factors in chicken intestinal epithelial cells in vitro. Frontiers in Microbiology 8, 2081.CrossRefGoogle ScholarPubMed
Haghighi, HR, Gong, J, Gyles, CL, Hayes, MA, Sanei, B, Parvizi, P, Gisavi, H, Chambers, JR and Sharif, S (2005) Modulation of antibody-mediated immune response by probiotics in chickens. Clinical and Diagnostic Laboratory Immunology 12, 1387–1392.Google ScholarPubMed
Hancock, REW, Haney, EF and Gill, EE (2016) The immunology of host defence peptides: beyond antimicrobial activity. Nature Reviews Immunology 16, 321–334.CrossRefGoogle ScholarPubMed
Hangalapura, BN, Nieuwland, MGB, Buyse, J, Kemp, B and Parmentier, HK (2004) Effect of duration of cold stress on plasma adrenal and thyroid hormone levels and immune responses in chicken lines divergently selected for antibody responses. Poultry Science 83, 1644–1649.CrossRefGoogle ScholarPubMed
Hegazy, WAH and Hensel, M (2012) Salmonella enterica as a vaccine carrier. Future Microbiology 7, 111–127.CrossRefGoogle ScholarPubMed
Hirakawa, R, Nurjanah, S, Furukawa, K, Murai, A, Kikusato, M, Nochi, T and Toyomizu, M (2020) Heat stress causes immune abnormalities via massive damage to effect proliferation and differentiation of lymphocytes in broiler chickens. Frontiers in Veterinary Science 7, 46.CrossRefGoogle ScholarPubMed
Hoang, TH, Hong, HA, Clark, GC, Titball, RW and Cutting, SM (2008) Recombinant Bacillus subtilis expressing the Clostridium perfringens alpha toxoid is a candidate orally delivered vaccine against necrotic enteritis. Infection and Immunity 76, 5257–5265.CrossRefGoogle ScholarPubMed
Hofacre, CL, Smith, JA and Mathis, GF (2018) An optimist's view on limiting necrotic enteritis and maintaining broiler gut health and performance in today's marketing, food safety, and regulatory climate. Poultry Science 97, 1929–1933.CrossRefGoogle ScholarPubMed
Hong, YH, Song, W, Lee, SH and Lillehoj, HS (2012) Differential gene expression profiles of β-defensins in the crop, intestine, and spleen using a necrotic enteritis model in 2 commercial broiler chicken lines. Poultry Science 91, 1081–1088.CrossRefGoogle ScholarPubMed
Jang, SI, Lillehoj, HS, Lee, S-H, Lee, KW, Lillehoj, EP, Hong, YH, An, D-J, Jeong, W, Chun, J-E and Bertrand, F (2012) Vaccination with Clostridium perfringens recombinant proteins in combination with MontanideTM ISA 71 VG adjuvant increases protection against experimental necrotic enteritis in commercial broiler chickens. Vaccine 30, 5401–5406.CrossRefGoogle Scholar
Jia, W, Slominski, BA, Bruce, HL, Blank, G, Crow, G and Jones, O (2009) Effects 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.CrossRefGoogle ScholarPubMed
Jiang, Y, Kulkarni, RR, Parreira, VR and Prescott, JF (2009) Immunization of broiler chickens against Clostridium perfringens-induced necrotic enteritis using purified recombinant immunogenic proteins. Avian Diseases 53, 409–415.CrossRefGoogle ScholarPubMed
Katalani, C, Ahmadian, G, Nematzadeh, G, Amani, J, Ehsani, P, Razmyar, J and Kiani, G (2020) Immunization with oral and parenteral subunit chimeric vaccine candidate confers protection against necrotic enteritis in chickens. Vaccine 38, 7284–7291.CrossRefGoogle ScholarPubMed
Keestra, AM, de Zoete, MR, Bouwman, LI, Vaezirad, MM and van Putten, JPM (2013) Unique features of chicken toll-like receptors. Developmental and Comparative Immunology 41, 316–323.CrossRefGoogle ScholarPubMed
Keyburn, AL, Boyce, JD, Vaz, P, Bannam, TL, Ford, ME, Parker, D, Di Rubbo, A, Rood, JI and Moore, RJ (2008) NetB, a new toxin that is associated with avian necrotic enteritis caused by Clostridium perfringens. PLoS Pathogens 4, e26.CrossRefGoogle ScholarPubMed
Keyburn, AL, Portela, RW, Ford, ME, Bannam, TL, Yan, XX, Rood, JI and Moore, RJ (2013 a) Maternal immunization with vaccines containing recombinant NetB toxin partially protects progeny chickens from necrotic enteritis. Veterinary Research 44, 1–7.Google ScholarPubMed
Keyburn, AL, Portela, RW, Sproat, K, Ford, ME, Bannam, TL, Yan, X, Rood, JI and Moore, RJ (2013 b) Vaccination with recombinant NetB toxin partially protects broiler chickens from necrotic enteritis. Veterinary Research 44, 1–8.Google ScholarPubMed
Kiu, R, Brown, J, Bedwell, H, Leclaire, C, Caim, S, Pickard, D, Dougan, G, Dixon, RA and Hall, LJ (2019) Genomic analysis on broiler-associated Clostridium perfringens strains and exploratory caecal microbiome investigation reveals key factors linked to poultry necrotic enteritis. Animal Microbiome 1, 1–14.CrossRefGoogle ScholarPubMed
Kodali, VP and Sen, R (2008) Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnology Journal : Healthcare, Nutrition, Technology 3, 245–251.CrossRefGoogle ScholarPubMed
Koenen, ME, Kramer, J, Van Der Hulst, R, Heres, L, Jeurissen, SHM and Boersma, WJA (2004) Immunomodulation by probiotic lactobacilli in layer- and meat-type chickens. British Poultry Science 45, 355–366.CrossRefGoogle ScholarPubMed
Kulkarni, RR, Parreira, VR, Sharif, S and Prescott, JF (2007) Immunization of broiler chickens against Clostridium perfringens-induced necrotic enteritis. Clinical and Vaccine Immunology 14, 1070–1077.CrossRefGoogle ScholarPubMed
Kulkarni, RR, Parreira, VR, Sharif, S and Prescott, JF (2008) Oral immunization of broiler chickens against necrotic enteritis with an attenuated Salmonella vaccine vector expressing Clostridium perfringens antigens. Vaccine 26, 4194–4203.CrossRefGoogle ScholarPubMed
Kulkarni, RR, Parreira, VR, Jiang, Y-F and Prescott, JF (2010) A live oral recombinant Salmonella enterica serovar Typhimurium vaccine expressing Clostridium perfringens antigens confers protection against necrotic enteritis in broiler chickens. Clinical and Vaccine Immunology 17, 205–214.CrossRefGoogle ScholarPubMed
Lacey, JA, Keyburn, AL, Ford, ME, Portela, RW, Johanesen, PA, Lyras, D and Moore, RJ (2017) Conjugation-mediated horizontal gene transfer of Clostridium perfringens plasmids in the chicken gastrointestinal tract results in the formation of new virulent strains. Applied and Environmental Microbiology 83, 1814–1817.CrossRefGoogle ScholarPubMed
Lacey, JA, Allnutt, TR, Vezina, B, Van, TTH, Stent, T, Han, X, Rood, JI, Wade, B, Keyburn, AL and Seemann, T (2018 a) Whole genome analysis reveals the diversity and evolutionary relationships between necrotic enteritis-causing strains of Clostridium perfringens. BMC Genomics 19, 1–22.CrossRefGoogle ScholarPubMed
Lacey, JA, Stanley, D, Keyburn, AL, Ford, M, Chen, H, Johanesen, P, Lyras, D and Moore, RJ (2018 b) Clostridium perfringens-mediated necrotic enteritis is not influenced by the pre-existing microbiota but is promoted by large changes in the post-challenge microbiota. Veterinary Microbiology 227, 119–126.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
La Ragione, RM, Narbad, A, Gasson, MJ and Woodward, MJ (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.CrossRefGoogle ScholarPubMed
Lepp, D, Roxas, B, Parreira, VR, Marri, PR, Rosey, EL, Gong, J, Songer, JG, Vedantam, G and Prescott, JF (2010) Identification of novel pathogenicity loci in Clostridium perfringens strains that cause avian necrotic enteritis. PLoS One 5, e10795.CrossRefGoogle ScholarPubMed
Levy, S (2014) Reduced antibiotic use in livestock: how Denmark tackled resistance. Environmental Health Perspectives 122, 160–165.CrossRefGoogle ScholarPubMed
Li, G, Lillehoj, HS, Lee, KW, Lee, SH, Park, MS, Jang, SI, Bauchan, GR, Gay, CG, Ritter, GD and Bautista, DA (2010) Immunopathology and cytokine responses in commercial broiler chickens with gangrenous dermatitis. Avian Pathology 39, 255–264.CrossRefGoogle ScholarPubMed
Li, GH, Hong, ZM, Jia, YJ, You, JM, Zhang, JH and Liu, BS (2012) Probiotic Lactobacilli stimulate avian beta-defensin 9 expression in cultured chicken small intestinal epithelial cells. Proceedings of the Nutrition Society 71, E239. doi:10.1017/S0029665112003308.CrossRefGoogle Scholar
Li, C, Yan, X and Lillehoj, HS (2017 a) Complete genome sequences of Clostridium perfringens Del1 strain isolated from chickens affected by necrotic enteritis. Gut Pathogens 9, 1–7.CrossRefGoogle ScholarPubMed
Li, Z, Wang, W, Liu, D and Guo, Y (2017 b) Effects of Lactobacillus acidophilus on gut microbiota composition in broilers challenged with Clostridium perfringens. PLoS One 12, e0188634.CrossRefGoogle ScholarPubMed
Lillehoj, HS and Lillehoj, EP (2000) Avian coccidiosis. A review of acquired intestinal immunity and vaccination strategies. Avian Diseases 44, 408–425.CrossRefGoogle ScholarPubMed
Lin, Y, Xu, S, Zeng, D, Ni, X, Zhou, M, Zeng, Y, Wang, H, Zhou, Y, Zhu, H and Pan, K (2017) Disruption in the cecal microbiota of chickens challenged with Clostridium perfringens and other factors was alleviated by Bacillus licheniformis supplementation. PLoS One 12, e0182426.CrossRefGoogle ScholarPubMed
Liu, JD, Lumpkins, B, Mathis, G, Williams, SM and Fowler, J (2019) Evaluation of encapsulated sodium butyrate with varying releasing times on growth performance and necrotic enteritis mitigation in broilers. Poultry Science 98, 3240–3245.CrossRefGoogle ScholarPubMed
Llanco, LA, Nakano, V, de Moraes, CTP, Piazza, RMF and Avila-Campos, MJ (2017) Adhesion and invasion of Clostridium perfringens type A into epithelial cells. Brazilian Journal of Microbiology 48, 764–768.CrossRefGoogle ScholarPubMed
Lovland, A, Kaldhusdal, M, Redhead, K, Skjerve, E and Lillehaug, A (2004) Maternal vaccination against subclinical necrotic enteritis in broilers. Avian Pathology 33, 81–90.CrossRefGoogle ScholarPubMed
Lu, Y, Sarson, AJ, Gong, J, Zhou, H, Zhu, W, Kang, Z, Yu, H, Sharif, S and Han, Y (2009) Expression profiles of genes in toll-like receptor-mediated signaling of broilers infected with Clostridium perfringens. Clinical and Vaccine Immunology 16, 1639–1647.CrossRefGoogle ScholarPubMed
MacMillan, JL, Vicaretti, SD, Noyovitz, B, Xing, X, Low, KE, Inglis, GD, Zaytsoff, SJM, Boraston, AB, Smith, SP and Uwiera, RRE (2019) Structural analysis of broiler chicken small intestinal mucin O-glycan modification by Clostridium perfringens. Poultry Science 98, 5074–5088.CrossRefGoogle ScholarPubMed
Martens, EC, Neumann, M and Desai, MS (2018) Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nature Reviews Microbiology 16, 457–470.CrossRefGoogle ScholarPubMed
Mattar, AF, Teiltelbaum, DH and Drongowski, RA (2003) Probiotics upregulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Journal of Pediatric Surgery 38, 1123.CrossRefGoogle Scholar
McDevitt, RM, Brooker, JD, Acamovic, T and Sparks, NHC (2006) Necrotic enteritis; a continuing challenge for the poultry industry. World's Poultry Science Journal 62, 221–247.CrossRefGoogle Scholar
Mishra, V, Shah, C, Mokashe, N, Chavan, R, Yadav, H and Prajapati, J (2015) Probiotics as potential antioxidants: a systematic review. Journal of Agricultural and Food Chemistry 63, 3615–3626.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
M'Sadeq, SA, Wu, S, Swick, RA and Choct, M (2015) Towards the control of necrotic enteritis in broiler chickens with in-feed antibiotics phasing-out worldwide. Animal Nutrition 1, 1–11.CrossRefGoogle ScholarPubMed
Nascimento, IP and Leite, LCC (2012) Recombinant vaccines and the development of new vaccine strategies. Brazilian Journal of Medical and Biological Research 45, 1102–1111.CrossRefGoogle ScholarPubMed
Navarro, MA, McClane, BA and Uzal, FA (2018) Mechanisms of action and cell death associated with Clostridium perfringens toxins. Toxins (Basel) 10, 212.CrossRefGoogle ScholarPubMed
Ng, SC, Hart, AL, Kamm, MA, Stagg, AJ and Knight, SC (2009) Mechanisms of action of probiotics: recent advances. Inflammatory Bowel Disease 15, 300–310.CrossRefGoogle ScholarPubMed
Palliyeguru, M, Rose, SP and Mackenzie, AM (2010) Effect of dietary protein concentrates on the incidence of subclinical necrotic enteritis and growth performance of broiler chickens. Poultry Science 89, 34–43.CrossRefGoogle ScholarPubMed
Parish, WE (1961) Necrotic enteritis in the fowl (Gall Us Gall Us D Omes Ticus): I. Histopathology of the disease and isolation of a strain of Clostridium welchii. Journal of Comparative Pathology and Therapeutics 71, 377–393.CrossRefGoogle Scholar
Parreira, VR, Russell, K, Athanasiadou, S and Prescott, JF (2016) Comparative transcriptome analysis by RNAseq of necrotic enteritis Clostridium perfringens during in vivo colonization and in vitro conditions. BMC Microbiology 16, 1–16.CrossRefGoogle ScholarPubMed
Pelaseyed, T, Bergström, JH, Gustafsson, JK, Ermund, A, Birchenough, GMH, Schütte, A, van der Post, S, Svensson, F, Rodríguez-Piñeiro, AM and Nyström, EEL (2014) The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunological Reviews 260, 8–20.CrossRefGoogle ScholarPubMed
Plantinga, TS, van Maren, WWC, van Bergenhenegouwen, J, Hameetman, M, Nierkens, S, Jacobs, C, de Jong, DJ, Joosten, LAB, van't Land, B and Garssen, J (2011) Differential Toll-like receptor recognition and induction of cytokine profile by Bifidobacterium breve and Lactobacillus strains of probiotics. Clinical and Vaccine Immunology 18, 621–628.CrossRefGoogle ScholarPubMed
Plaza-Díaz, J, Ruiz-Ojeda, FJ, Vilchez-Padial, LM and Gil, A (2017) Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients 9, 555.CrossRefGoogle ScholarPubMed
Prescott, JF, Parreira, VR, Mehdizadeh Gohari, I, Lepp, D and Gong, J (2016) The pathogenesis of necrotic enteritis in chickens: what we know and what we need to know: a review. Avian Pathology 45, 288–294.CrossRefGoogle ScholarPubMed
Qing, X, Zeng, D, Wang, H, Ni, X, Liu, L, Lai, J, Khalique, A, Pan, K and Jing, B (2017) Preventing subclinical necrotic enteritis through Lactobacillus johnsonii BS15 by ameliorating lipid metabolism and intestinal microflora in broiler chickens. AMB Express 7, 1–12.CrossRefGoogle ScholarPubMed
Regnier, JA and Kelley, KW (1981) Heat-and cold-stress suppresses in vivo and in vitro cellular immune responses of chickens. American Journal of Veterinary Research 42, 294–299.Google ScholarPubMed
Rehman, H, Awad, WA, Lindner, I, Hess, M and Zentek, J (2006) Clostridium perfringens alpha toxin affects electrophysiological properties of isolated jejunal mucosa of laying hens. Poultry Science 85, 1298–1302.CrossRefGoogle ScholarPubMed
Rehman, H, Ijaz, A, Specht, A, Dill, D, Hellweg, P, Männer, K and Zentek, J (2009) In vitro effects of alpha toxin from Clostridium perfringens on the electrophysiological parameters of jejunal tissues from laying hens preincubated with inulin and N-acetyl-L-cysteine. Poultry Science 88, 199–204.CrossRefGoogle ScholarPubMed
Rhayat, L, Maresca, M, Nicoletti, C, Perrier, J, Brinch, KS, Christian, S, Devillard, E and Eckhardt, E (2019) Effect of Bacillus subtilis strains on intestinal barrier function and inflammatory response. Frontiers in Immunology 10, 564.CrossRefGoogle ScholarPubMed
Robinson, K, Chamberlain, LM, Schofield, KM, Wells, JM and Le Page, RWF (1997) Oral vaccination of mice against tetanus with recombinant Lactococcus lactis. Nature Biotechnology 15, 653–657.CrossRefGoogle ScholarPubMed
Ronco, T, Stegger, M, Ng, KL, Lilje, B, Lyhs, U, Andersen, PS and Pedersen, K (2017) Genome analysis of Clostridium perfringens isolates from healthy and necrotic enteritis infected chickens and turkeys. BMC Research Notes 10, 1–6.CrossRefGoogle ScholarPubMed
Rood, JI, Keyburn, AL and Moore, RJ (2016) NetB and necrotic enteritis: the hole movable story. Avian Pathology 45, 295–301.CrossRefGoogle ScholarPubMed
Rood, JI, Adams, V, Lacey, J, Lyras, D, McClane, BA, Melville, SB, Moore, RJ, Popoff, MR, Sarker, MR and Songer, JG (2018) Expansion of the Clostridium perfringens toxin-based typing scheme. Anaerobe 53, 5–10.CrossRefGoogle ScholarPubMed
Rosique, RM, Chamignon, C, Mhedbi-Hajri, N, Chain, F, Derrien, M, Vazquez, UE, Garault, P, Cotillard, A, Pham, HP and Chervaux, C (2019) The potential probiotic Lactobacillus rhamnosus CNCM 1-3690 strain protects the intestinal barrier by stimulating both mucus production and cytoprotective response. Scientific Reports 9, 1–14.Google Scholar
Russell, JB and Diez-Gonzalez, F (1997) The effects of fermentation acids on bacterial growth. Advances in Microbial Physiology 39, 205–234.CrossRefGoogle Scholar
Saleh, N, Nabil, R, Fathalla, S and Mosaad, A (2010) Clinicopathological and immunological studies on Toxoid vaccine as a successful alternative in controlling clostridial infection in broilers. Journal of Veterinary Medicine and Research 20, 106–115.CrossRefGoogle Scholar
Savva, CG, da Costa, SPF, Bokori-Brown, M, Naylor, CE, Cole, AR, Moss, DS, Titball, RW and Basak, AK (2013) Molecular architecture and functional analysis of NetB, a pore-forming toxin from Clostridium perfringens. Journal of Biological Chemistry 288, 3512–3522.CrossRefGoogle ScholarPubMed
Schlee, M, Harder, J, Köten, B, Stange, EF, Wehkamp, J and Fellermann, K (2008) Probiotic lactobacilli and VSL# 3 induce enterocyte β-defensin 2. Clinical & Experimental Immunology 151, 528–535.CrossRefGoogle ScholarPubMed
Shojadoost, B, Vince, AR and Prescott, JF (2012) The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: a critical review. Veterinary Research 43, 1–12.CrossRefGoogle ScholarPubMed
Smyth, JA (2016) Pathology and diagnosis of necrotic enteritis: is it clear-cut? Avian Pathology 45, 282–287.CrossRefGoogle ScholarPubMed
Song, B, Li, H, Wu, Y, Zhen, W, Wang, Z, Xia, Z and Guo, Y (2017) Effect of microencapsulated sodium butyrate dietary supplementation on growth performance and intestinal barrier function of broiler chickens infected with necrotic enteritis. Animal Feed Science and Technology 232, 6–15.CrossRefGoogle Scholar
Songer, JG (1996) Clostridial enteric diseases of domestic animals. Clinical Microbiology Reviews 9, 216.CrossRefGoogle ScholarPubMed
Sornplang, P and Leelavatcharamas, V (2010) Antimicrobial susceptibility of probiotic lactobacilli isolated from chicken feces. Asia-Pacific Journal of Science and Technology 15, 689–697.Google Scholar
Sugiarto, H and Yu, P-L (2004) Avian antimicrobial peptides: the defense role of β-defensins. Biochemical and Biophysical Research Communications 323, 721–727.CrossRefGoogle ScholarPubMed
Sugimura, T, Jounai, K, Ohshio, K, Tanaka, T, Suwa, M and Fujiwara, D (2013) Immunomodulatory effect of Lactococcus lactis JCM5805 on human plasmacytoid dendritic cells. Clinical Immunology 149, 509–518.CrossRefGoogle ScholarPubMed
Sun, Y and O'Riordan, MXD (2013) Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Advances in Applied Microbiology 85, 93–118.CrossRefGoogle ScholarPubMed
Taha-abdelaziz, K, Alkie, TN, Hodgins, DC, Shojadoost, B and Sharif, S (2016) Characterization of host responses induced by Toll-like receptor ligands in chicken cecal tonsil cells. Veterinary Immunology and Immunopathology 174, 19–25.CrossRefGoogle ScholarPubMed
Teo, AY-L 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 and Environmental Microbiology 71, 4185–4190.CrossRefGoogle ScholarPubMed
Thompson, DR, Parreira, VR, Kulkarni, RR and Prescott, JF (2006) Live attenuated vaccine-based control of necrotic enteritis of broiler chickens. Veterinary Microbiology 113, 25–34.CrossRefGoogle ScholarPubMed
Tsiouris, V (2016) Poultry management: a useful tool for the control of necrotic enteritis in poultry. Avian Pathology 45, 323–325.CrossRefGoogle ScholarPubMed
Tsiouris, V, Georgopoulou, I, Batzios, C, Pappaioannou, N, Ducatelle, R and Fortomaris, P (2015) High stocking density as a predisposing factor for necrotic enteritis in broiler chicks. Avian Pathology 44, 59–66.CrossRefGoogle ScholarPubMed
Tsiouris, V, Georgopoulou, I, Batzios, C, Pappaioannou, N, Ducatelle, R and Fortomaris, P (2018) Heat stress as a predisposing factor for necrotic enteritis in broiler chicks. Avian Pathology 47, 616–624.CrossRefGoogle ScholarPubMed
van der Wielen, PWJJ, Biesterveld, S, Notermans, S, Hofstra, H, Urlings, BAP and van Knapen, F (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Applied and Environmental Microbiology 66, 2536–2540.CrossRefGoogle ScholarPubMed
van Dijk, A, Veldhuizen, EJA, Kalkhove, SIC, Tjeerdsma-van Bokhoven, JLM, Romijn, RA and Haagsman, HP (2007) The β-defensin gallinacin-6 is expressed in the chicken digestive tract and has antimicrobial activity against food-borne pathogens. Antimicrobial Agents and Chemotherapy 51, 912–922.CrossRefGoogle ScholarPubMed
van Dijk, A, Veldhuizen, EJA and Haagsman, HP (2008) Avian defensins. Veterinary Immunology and Immunopathology 124, 1–18.CrossRefGoogle ScholarPubMed
Vermette, D, Hu, P, Canarie, MF, Funaro, M, Glover, J and Pierce, RW (2018) Tight junction structure, function, and assessment in the critically ill: a systematic review. Intensive Care Medicine Experimental 6, 1–18.CrossRefGoogle ScholarPubMed
Wade, B, Keyburn, AL, Seemann, T, Rood, JI and Moore, RJ (2015) Binding of Clostridium perfringens to collagen correlates with the ability to cause necrotic enteritis in chickens. Veterinary Microbiology. 180, 299–303.CrossRefGoogle ScholarPubMed
Wade, B, Keyburn, AL, Haring, V, Ford, M, Rood, JI and Moore, RJ (2016) The adherent abilities of Clostridium perfringens strains are critical for the pathogenesis of avian necrotic enteritis. Veterinary Microbiology 197, 53–61.CrossRefGoogle ScholarPubMed
Wade, B, Keyburn, AL, Haring, V, Ford, M, Rood, JI and Moore, RJ (2020) Two putative zinc metalloproteases contribute to the virulence of Clostridium perfringens strains that cause avian necrotic enteritis. Journal of Veterinary Diagnostic Investigation 32, 259–267.CrossRefGoogle Scholar
Walliser, I and Göbel, TW (2018) Chicken IL-17A is expressed in αβ and γδ T cell subsets and binds to a receptor present on macrophages, and T cells. Developmental and Comparative Immunology 81, 44–53.CrossRefGoogle ScholarPubMed
Wang, H, Ni, X, Qing, X, Liu, L, Lai, J, Khalique, A, Li, G, Pan, K, Jing, B and Zeng, D (2017) Probiotic enhanced intestinal immunity in broilers against subclinical necrotic enteritis. Frontiers in Immunology 8, 1592.CrossRefGoogle ScholarPubMed
Wang, B, Hussain, A, Zhou, Y, Zeng, Z, Wang, Q, Zou, P, Gong, L, Zhao, P and Li, W (2020) Saccharomyces boulardii attenuates inflammatory response induced by Clostridium perfringens via TLR4/TLR15-MyD8 pathway in HD11 avian macrophages. Poultry Science 99, 5356–5365.CrossRefGoogle ScholarPubMed
Wilde, S, Jiang, Y, Tafoya, AM, Horsman, J, Yousif, M, Vazquez, LA and Roland, KL (2019) Salmonella-vectored vaccine delivering three Clostridium perfringens antigens protects poultry against necrotic enteritis. PLoS One 14, e0197721.CrossRefGoogle ScholarPubMed
Williams, RB (2005) Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathology 34, 159–180.CrossRefGoogle ScholarPubMed
Woo, J and Ahn, J (2013) Probiotic-mediated competition, exclusion and displacement in biofilm formation by food-borne pathogens. Letters in Applied Microbiology 56, 307–313.CrossRefGoogle ScholarPubMed
Wu, Y, Zhen, W, Geng, Y, Wang, Z and Guo, Y (2019) Pretreatment with probiotic Enterococcus faecium NCIMB 11181 ameliorates necrotic enteritis-induced intestinal barrier injury in broiler chickens. Scientific Reports 9, 1–17.Google ScholarPubMed
Xu, T, Chen, Y, Yu, L, Wang, J, Huang, M and Zhu, N (2020) Effects of Lactobacillus plantarum on intestinal integrity and immune responses of egg-laying chickens infected with Clostridium perfringens under the free-range or the specific pathogen free environment. BMC Veterinary Research 16, 47.CrossRefGoogle ScholarPubMed
Xue, G-D, Wu, S-B, Choct, M and Swick, RA (2017) The role of supplemental glycine in establishing a subclinical necrotic enteritis challenge model in broiler chickens. Animal Nutrition 3, 266–270.CrossRefGoogle ScholarPubMed
Yan, F and Polk, DB (2011) Probiotics and immune health. Current Opinion in Gastroenterology 27, 496.CrossRefGoogle ScholarPubMed
Yang, WY, Chou, CH and Wang, C (2018) Characterization of toxin genes and quantitative analysis of netB in necrotic enteritis (NE)-producing and non-NE-producing Clostridium perfringens isolated from chickens. Anaerobe 54, 115–120.CrossRefGoogle ScholarPubMed
Yitbarek, A, Echeverry, H, Brady, J, Hernandez-Doria, J, Camelo-Jaimes, G, Sharif, S, Guenter, W, House, JD and Rodriguez-Lecompte, JC (2012) Innate immune response to yeast-derived carbohydrates in broiler chickens fed organic diets and challenged with Clostridium perfringens. Poultry Science 91, 1105–1112.CrossRefGoogle ScholarPubMed
Yu, Q, Lepp, D, Gohari, IM, Wu, T, Zhou, H, Yin, X, Yu, H, Prescott, JF, Nie, S-P and Xie, M-Y (2017) The Agr-like quorum sensing system is required for pathogenesis of necrotic enteritis caused by Clostridium perfringens in poultry. Infection and Immunity 85, 975–991.CrossRefGoogle ScholarPubMed
Zacharof, MP and Lovitt, RW (2012) Bacteriocins produced by lactic acid bacteria a review article. APCBEE Procedia 2, 50–56.CrossRefGoogle Scholar
Zekarias, B, Mo, H and Curtiss, R (2008) 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. Clinical and Vaccine Immunology 15, 805–816.CrossRefGoogle ScholarPubMed
Zhang, B, Lv, Z, Li, H, Guo, S, Liu, D and Guo, Y (2017 a) Dietary l-arginine inhibits intestinal Clostridium perfringens colonisation and attenuates intestinal mucosal injury in broiler chickens. British Journal of Nutrition 118, 321–332.CrossRefGoogle ScholarPubMed
Zhang, W, Wang, P, Wang, B, Ma, B and Wang, J (2017 b) A combined Clostridium perfringens/Trueperella pyogenes inactivated vaccine induces complete immunoprotection in a mouse model. Biologicals 47, 1–10.CrossRefGoogle ScholarPubMed
Zhou, M, Zeng, D, Ni, X, Tu, T, Yin, Z, Pan, K and Jing, B (2016) Effects of Bacillus licheniformis on the growth performance and expression of lipid metabolism-related genes in broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Lipids in Health and Disease 15, 1–10.CrossRefGoogle ScholarPubMed
Zhou, H, Lepp, D, Pei, Y, Liu, M, Yin, X, Ma, R, Prescott, JF and Gong, J (2017) Influence of pCP1NetB ancillary genes on the virulence of Clostridium perfringens poultry necrotic enteritis strain CP1. Gut Pathogens 9, 1–7.CrossRefGoogle ScholarPubMed