A Meta-analysis of Antimicrobial Peptide Effects on Intestinal Bacteria, Immune Response, and Antioxidant Activity of Broilers

M. M. Sholikin, A. T. Wahyudi, A. Jayanegara, J. Nomura, Nahrowi Nahrowi

Abstract

This study used a meta-analysis to systematically assess the effect of antimicrobial peptide (AMP) addition on the number of bacteria, immune responses, and antioxidant activity of broilers. The database was compiled from 29 post evaluation articles that were found in search engines consisted of 36 experiments and 111 data. The mixed model method was used to assess the effect of AMP, with AMP addition level as a fixed effect and experiment as a random effect. The fixed effect was tested for linear and quadratic models. The quadratic model was retained when significant at p<0.05 but turned into its corresponding linear model when insignificant. In the starter phase, AMP addition decreased the number of bacteria in the ileum (coliform and total aerobic bacteria (TAB); (p<0.05), the caecum (Clostridium spp., Escherichia coli, coliform, and lactic acid bacteria (LAB); p<0.05), and excreta (Clostridium spp.; p<0.1). Similarly, the number of bacteria also declined in the ileum (Escherichia coli, p<0.05; TAB, p<0.1), the caecum (LAB; p<0.1), and excreta (Clostridium spp.; p<0.05) of broilers in the finisher phase. There were significant improvements in immune response and antioxidant activity in starter broiler, as indicated by the titer of Newcastle disease (ND) antibody, bursal index, spleen index, and thymus index (p<0.05) due to AMP addition. Variables of immunoglobulin M (IgM), cluster of differentiation 4 (CD4), ND antibody titer, bursal index, spleen index, and thymus index were also significantly increased (p<0.05) while superoxide dismutase activity (SOD activity) tended to increase (p<0.1) in finisher broiler following the AMP addition. In short, AMP addition is able to suppress the number of pathogenic bacteria and increase the immune response and antioxidant activity of broilers.

References

Abdel-Latif, M. A., A. H. El-Far, A. R. Elbestawy, R. Ghanem, S. A. Mousa, & H. S. Abd El-Hamid. 2017. Exogenous dietary lysozyme improves the growth performance and gut microbiota in broiler chickens targeting the antioxidant and non-specific immunity mRNA expression. PLoS ONE. 12:1-17. https://doi.org/10.1371/journal.pone.0185153
Aguirre, A. T. A., S. P. Acda, A. A. Angeles, M. C. R. Oliveros, F. E. Merca, & F. A. Cruz. 2015. Effect of Bovine Lactoferrin on growth performance and intestinal histologic features of broilers. Philipp. J. Vet. Anim. Sci. 41:12-20.
Ali, A. & K. Mohanny. 2014. Effect of injection with bee venom extract on productive performance and immune response of broiler chicks. Journal of Animal and Poultry Production. 5:237-246. https://doi.org/10.21608/jappmu.2014.69561
Aliakbarpour, H. R., M. Chamani, G. Rahimi, A. A. Sadeghi, & D. Qujeq. 2012. The Bacillus subtilis and lactic acid bacteria probiotics influences intestinal mucin gene expression, histomorphology and growth performance in broilers. Asian-Australas. J. Anim. Sci. 25:1285-1293. https://doi.org/10.5713/ajas.2012.12110
Anabrees, J., F. Indrio, B. Paes, & K. AlFaleh. 2013. Probiotics for infantile colic: A systematic review. BMC Pediatr. 13:186. https://doi.org/10.1186/1471-2431-13-186
Askelson, T. E., C. A. Flores, S. L. Dunn-Horrocks, Y. Dersjant-Li, K. Gibbs, A. Awati, J. T. Lee, & T. Duong. 2018. Effects of direct-fed microorganisms and enzyme blend co-administration on intestinal bacteria in broilers fed diets with or without antibiotics. Poult. Sci. 97:54-63. https://doi.org/10.3382/ps/pex270
Bahar, A. & D. Ren. 2013. Antimicrobial peptides. Pharmaceuticals. 6: 1543-1575. https://doi.org/10.3390/ph6121543
Bai, J., R. Wang, L. Yan, & J. Feng. 2019. Co-supplementation of dietary seaweed powder and antibacterial peptides improves broiler growth performance and immune function. Braz. J. Poult. Sci. 21:1-9. https://doi.org/10.1590/1806-9061-2018-0826
Bao, H., R. She, T. Liu, Y. Zhang, K. S. Peng, D. Luo, Z. Yue, Y. Ding, Y. Hu, W. Liu, & L. Zhai. 2009. Effects of pig antibacterial peptides on growth performance and intestine mucosal immune of broiler chickens. Poult. Sci. 88:291-297. https://doi.org/10.3382/ps.2008-00330
Bates, D., M. Mächler, B. Bolker, & S. Walker. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67:1-48. https://doi.org/10.18637/jss.v067.i01
Bauer, E., S. Jakob, & R. Mosenthin. 2005. Principles of physiology of lipid digestion. Asian-Australas. J. Anim. Sci. 18:282-295. https://doi.org/10.5713/ajas.2005.282
Bonner, A., A. Almogren, P. B. Furtado, M. A. Kerr, & S. J. Perkins. 2009. Location of secretory component on the Fc edge of dimeric IgA1 reveals insight into the role of secretory IgA1 in mucosal immunity. Mucosal Immunol. 2:74-84. https://doi.org/10.1038/mi.2008.68
Bradshaw, J. P. 2003. Cationic antimicrobial peptides: Issues for potential clinical use. BioDrugs. 17:233-240. https://doi.org/10.2165/00063030-200317040-00002
Caldwell, D. J., H. D. Danforth, B. C. Morris, K. A. Ameiss, & A. P. McElroy. 2004. Participation of the intestinal epithelium and mast cells in local mucosal immune responses in commercial poultry. Poul. Sci. 83:591-599. https://doi.org/10.1093/ps/83.4.591
Chai, T. & R. R. Draxler. 2014. Root mean square error (RMSE) or mean absolute error (MAE)? - Arguments against avoiding RMSE in the literature. Geosci. Model Dev. 7:1247-1250. https://doi.org/10.5194/gmd-7-1247-2014
Chalk, C. H., T. J. Benstead, J. D. Pound, & M. R. Keezer. 2019. Medical treatment for botulism. Cochrane Database of Sys. Rev. 4:1465-1858. https://doi.org/10.1002/14651858.CD008123.pub4
Choi, S. C., S. L. Ingale, J. S. Kim, Y. K. Park, I. K. Kwon, & B. J. Chae. 2013a. An antimicrobial peptide-A3: Effects on growth performance, nutrient retention, intestinal and faecal microflora and intestinal morphology of broilers. Br. Poult. Sci. 54:738-746. https://doi.org/10.1080/00071668.2013.838746
Choi, S. C., S. L. Ingale, J. S. Kim, Y. K. Park, I. K. Kwon, & B. J. Chae. 2013b. Effects of dietary supplementation with an antimicrobial peptide-P5 on growth performance, nutrient retention, excreta and intestinal microflora and intestinal morphology of broilers. Anim. Feed Sci. Technol. 185:78-84. https://doi.org/10.1016/j.anifeedsci.2013.07.005
Chowdhury, S., G. P. Mandal, A. K. Patra, P. Kumar, I. Samanta, S. Pradhan, & A. K. Samanta. 2018. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim. Feed Sci. Technol. 236:39-47. https://doi.org/10.1016/j.anifeedsci.2017.12.003
Corpas, F. J., A. Fernández-Ocaña, A. Carreras, R. Valderrama, F. Luque, F. J. Esteban, M. Rodríguez-Serrano, M. Chaki, J. R. Pedrajas, L. M. Sandalio, L. A. del Río, & J. B. Barroso. 2006. The expression of different superoxide dismutase forms is cell-type dependent in olive (Olea europaea L.) leaves. Plant Cell Physiol. 47:984-994. https://doi.org/10.1093/pcp/pcj071
Daneshmand, A., H. Kermanshahi, M. H. Sekhavati, A. Javadmanesh, & M. Ahmadian. 2019a. Antimicrobial peptide, cLF36, affects performance and intestinal morphology, microflora, junctional proteins, and immune cells in broilers challenged with E. coli. Sci. Rep. 9:14176. https://doi.org/10.1038/s41598-019-50511-7
Daneshmand, A., H. Kermanshahi, M. H. H. Sekhavati, A. Javadmanesh, M. Ahmadian, M. Alizadeh, & A. Aldavoodi. 2019b. Effects of cLF-chimera, a recombinant antimicrobial peptide, on intestinal morphology, microbiota, and gene expression of immune cells and tight junctions in broiler chickens challenged with C. perfringens. BioRxiv. 2019:1-34. https://doi.org/10.1101/871467
Enany, M., A. E. A. El Gammal, R. Solimane, A. El Sissi, & A. Hebashy. 2017. Evaluation of lactoferrin immunomodulatory effect on the immune response of broiler chickens. Suez Canal Veterinary Medicine Journal. 22:135-146. https://doi.org/10.21608/scvmj.2017.62452
Fagarasan, S. & T. Honjo. 2003. Intestinal IgA synthesis: Regulation of front-line body defences. Nat. Rev. Immunol. 3:63-72. https://doi.org/10.1038/nri982
Gadde, U., W. H. Kim, S. T. Oh, & H. S. Lillehoj. 2017. Alternatives to antibiotics for maximizing growth performance and feed efficiency in poultry: A review. Anim. Health Res. Rev. 18:26-45. https://doi.org/10.1017/S1466252316000207
Gałecki, A. & T. Burzykowski. 2013. Linear Mixed-Effects Models Using R. Springer New York. New York, NY. https://doi.org/10.1007/978-1-4614-3900-4

Geier, M. S., V. A. Torok, P. Guo, G. E. Allison, M. Boulianne, V. Janardhana, A. G. D. Bean, & R. J. Hughes. 2011. The effects of Lactoferrin on the intestinal environment of broiler chickens. Br. Poult. Sci. 52:564-572. https://doi.org/10.1080/00071668.2011.607429
Girard, M. & G. Bee. 2020. Invited review: Tannins as a potential alternative to antibiotics to prevent coliform diarrhea in weaned pigs. Animal. 14:95-107. https://doi.org/10.1017/S1751731119002143
Gong, M., D. Anderson, B. Rathgeber, & J. MacIsaac. 2017. The effect of dietary lysozyme with EDTA on growth performance and intestinal microbiota of broiler chickens in each period of the growth cycle. J. Appl. Poult. Res. 26:1-8. https://doi.org/10.3382/japr/pfw041
Han, S. M., K. G. Lee, J. H. Yeo, B. Y. Oh, B. S. Kim, W. Lee, H. J. Baek, S. T. Kim, S. J. Hwang, & S. C. Pak. 2010. Effects of honeybee venom supplementation in drinking water on growth performance of broiler chickens. Poult. Sci. 89:2396-2400. https://doi.org/10.3382/ps.2010-00915
Hu, X. F., Y. M. Guo, B. Y. Huang, S. Bun, L. B. Zhang, J. H. Li, D. Liu, F. Y. Long, X. Yang, & P. Jiao. 2010. The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poult. Scie. 89:1967-1974. https://doi.org/10.3382/ps.2009-00547
Hurwitz, S., A. Bar, M. Katz, D. Sklan, & P. Budowski. 1973. Absorption and secretion of fatty acids and bile acids in the intestine of the laying fowl. J Nutr. 103:543-547. https://doi.org/10.1093/jn/103.4.543
Ikeda, Y. 2001. PR-39, a Proline/Arginine-rich antimicrobial peptide, exerts cardioprotective effects in myocardial ischemia-reperfusion. Cardiovasc. Res. 49:69-77. https://doi.org/10.1016/S0008-6363(00)00226-1
Jazayeri, M. H., M. Sadri, A. Mostafaie, & R. Nedaeinia. 2019. Identification of an Immunoglobulin M (IgM) antibody against Enolase 1 protein (ENO1) derived from HEK-293 cells in patients with kidney failureInt. J. Pept. Res. Ther. 26:1251-1257. https://doi.org/10.1007/s10989-019-09919-y
Jiang, Y. B., Q. Q. Yin, & Y. R. Yang. 2009. Effect of soybean peptides on growth performance, intestinal structure and mucosal immunity of broilers. J Anim. Physiol. Anim. Nutr. 93:754-760. https://doi.org/10.1111/j.1439-0396.2008.00864.x
Joerger, R. 2003. Alternatives to antibiotics: Bacteriocins, antimicrobial peptides and bacteriophages. Poult. Sci. 82:640-647. https://doi.org/10.1093/ps/82.4.640
Johnson, E. A. 2019. Clostridium botulinum; p. 487-512. In Food Microbiology. ASM Press, Washington, DC, USA. https://doi.org/10.1128/9781555819972.ch18
Józefiak, D., A. Józefiak, B. Kierończyk, M. Rawski, S. Świątkiewicz, J. Długosz, & R. M. Engberg. 2016. Insects - A natural nutrient source for poultry - A review. Ann. Anim. Sci. 16:297-313. https://doi.org/10.1515/aoas-2016-0010
Karimzadeh, S., R. M. & A. T. Yansari. 2016. Effects of canola bioactive peptides on performance, digestive enzyme activities, nutrient digestibility, intestinal morphology and gut microflora in broiler chickens. Poult. Sci. J. 4:27-36.
Karimzadeh, S., M. Rezaei, & A. Teimouri-Yansari. 2017a. Effect of canola peptides, antibiotic, probiotic and prebiotic on performance, digestive enzymes activity and some ileal aerobic bacteria in broiler chicks. Iranian Journal of Animal Science. 48:129-139. https://doi.org/10.22059/ijas.2017.221313.653481
Karimzadeh, S., M. Rezaei, & A. T. Yansari. 2017b. Effects of different levels of canola meal peptides on growth performance and blood metabolites in broiler chickens. Livest. Sci. 203:37-40. https://doi.org/10.1016/j.livsci.2017.06.013
Kierończyk, B., M. Rawski, Z. Mikołajczak, S. Świątkiewicz, & D. Józefiak. 2020. Nisin as a novel feed additive: The effects on gut microbial modulation and activity, histological parameters, and growth performance of broiler chickens. Animals. 10:101. https://doi.org/10.3390/ani10010101
Kim, D. H., S. M. Han, M. C. Keum, S. Lee, B. K. An, S.-R. Lee, & K.-W. Lee. 2018. Evaluation of bee venom as a novel feed additive in fast-growing broilers. Br. Poult. Sci. 59:435-442. https://doi.org/10.1080/00071668.2018.1476675
Kim, J.-Y., S.-C. Park, M.-H. Kim, H.-T. Lim, Y. Park, & K. Hahm. 2005. Antimicrobial activity studies on a trypsin-chymotrypsin protease inhibitor obtained from potato. Biochem. Biophys. Res. Commun. 330:921-927. https://doi.org/10.1016/j.bbrc.2005.03.057
King, M. R., V. Ravindran, P. C. H. Morel, D. V. Thomas, M. J. Birtles, & J. R. Pluske. 2005. Effects of spray-dried colostrum and plasmas on the performance and gut morphology of broiler chickens. Aust. J. Agric. Res. 56:811. https://doi.org/10.1071/AR04324
Kogut, M. H. 2019. The effect of microbiome modulation on the intestinal health of poultry. Anim. Feed Sci. Technol. 250:32-40. https://doi.org/10.1016/j.anifeedsci.2018.10.008
Krajmalnik-Brown, R., Z. Ilhan, D. Kang, & J. K. DiBaise. 2012. Effects of gut microbes on nutrient absorption and energy regulation. Nutr. Clin. Pract. 27:201-214. https://doi.org/10.1177/0884533611436116
Leeson, S. & J. D. Summers. 2009. Commercial Poultry Nutrition. Third Edition. Nottingham University Press, Nottingham, UK. https://doi.org/10.7313/UPO9781904761099
Li, Y., Q. Xiang, Q. Zhang, Y. Huang, & Z. Su. 2012. Overview on the recent study of antimicrobial peptides: Origins, functions, relative mechanisms and application. Peptides. 37:207-215. https://doi.org/10.1016/j.peptides.2012.07.001
Li, Z., R. Mao, D. Teng, Y. Hao, H. Chen, X. Wang, X. Wang, N. Yang, & J. Wang. 2017. Antibacterial and immunomodulatory activities of insect Defensins (DLP2 and DLP4) against multidrug-resistant Staphylococcus aureus. Sci. Rep. 7:12124. https://doi.org/10.1038/s41598-017-10839-4
Liu, D., Y. Guo, Z. Wang, & J. Yuan. 2010. Exogenous Lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathol. 39:17-24. https://doi.org/10.1080/03079450903447404
Lu, J., U. Idris, B. Harmon, C. Hofacre, J. J. Maurer, & M. D. Lee. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl. Environ. Microbiol. 69:6816-6824. https://doi.org/10.1128/AEM.69.11.6816-6824.2003
Lüders, T., G. A. Birkemo, G. Fimland, J. Nissen-Meyer, & I. F. Nes. 2003. Strong synergy between a eukaryotic antimicrobial peptide and bacteriocins from lactic acid bacteria. Appl. Environ. Microbiol. 69:1797-1799. https://doi.org/10.1128/AEM.69.3.1797-1799.2003
Ma, J. L., L. H. Zhao, D. D. Sun, J. Zhang, Y. P. Guo, Z. Q. Zhang, Q. G. Ma, C. Ji, & L. H. Zhao. 2020. Effects of dietary supplementation of recombinant plectasin on growth performance, intestinal health and innate immunity response in broilers. Probiotics Antimicrob. Proteins. 12:214-223. https://doi.org/10.1007/s12602-019-9515-2
Macpherson, A. J., & E. Slack. 2007. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr. Opin. Gastroenterol. 23:673-678. https://doi.org/10.1097/MOG.0b013e3282f0d012
Malcolm, J. F. 1938. The classification of coliform bacteria. Epidemiol. Infect. 38:395-423. https://doi.org/10.1017/S0022172400011281
Murguia-Favela, L., N. Sharfe, A. Karanxha, A. Bates, H. Dadi, L. Cimpean, & C. M. Roifman. 2017. CD40 deficiency: A unique adult patient with hyper Immunoglobulin M syndrome and normal expression of CD40. LymphoSign Journal. 4:lymphosign-2017-0004. https://doi.org/10.14785/lymphosign-2017-0004
Ohh, S. H., P. L. Shinde, Z. Jin, J. Y. Choi, T.-W. Hahn, H. T. Lim, G. Y. Kim, Y. Park, K.-S. Hahm, & B. J. Chae. 2009. Potato (Solanum tuberosum L. cv. Gogu valley) protein as an antimicrobial agent in the diets of broilers. Poult. Sci. 88:1227-1234. https://doi.org/10.3382/ps.2008-00491
Park, S., & S. M. Yoe. 2017a. A novel Cecropin-like peptide from black soldier fly, Hermetia illucens : Isolation, structural, and functional characterization. Entomol. Res. 47:115-124. https://doi.org/10.1111/1748-5967.12226
Park, S., & S. M. Yoe. 2017b. Defensin-like peptide3 from black solder fly: Identification, characterization, and key amino acids for anti-Gram-negative bacteria. Entomol. Res. 47: 41-47. https://doi.org/10.1111/1748-5967.12214
Pellegrini, A., U. Thomas, R. von Fellenberg, & P. Wild. 1992. Bactericidal activities of Lysozyme and Aprotinin against Gram-negative and Gram-positive bacteria related to their basic character. J. Appl. Microbiol. 72:180-187. https://doi.org/10.1111/j.1365-2672.1992.tb01821.x
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, EISPACK, S. Heisterkamp, B. Van Willigen, & R-core. 2020. Linear and Nonlinear Mixed Effects Models. 1-335 p.
Ragland, S. A. & A. K. Criss. 2017. From bacterial killing to immune modulation: Recent insights into the functions of Lysozyme. PLoS Pathog. 13:e1006512. https://doi.org/10.1371/journal.ppat.1006512
Ren, Z. H., W. Yuan, H. D. Deng, J. L. Deng, Q. X. Dan, H. T. Jin, C. L. Tian, X. Peng, Z. Liang, S. Gao, S. H. Xu, G. Li, & Y. Hu. 2015. Effects of antibacterial peptide on cellular immunity in weaned piglets. J. Anim. Sci. 93:127-134. https://doi.org/10.2527/jas.2014-7933
Rowland, I., G. Gibson, A. Heinken, K. Scott, J. Swann, I. Thiele, & K. Tuohy. 2018. Gut microbiota functions: Metabolism of nutrients and other food components. Eur. J. Nutr. 57:1-24. https://doi.org/10.1007/s00394-017-1445-8
Salavati, M. E., V. Rezaeipour, R. Abdullahpour, & N. Mousavi. 2019. Effects of graded inclusion of bioactive peptides derived from sesame meal on the growth performance, internal organs, gut microbiota and intestinal morphology of broiler chickens. Int. J. Pept. Res. Ther. 26:1541-1548. https://doi.org/10.1007/s10989-019-09947-8
Sauvant, D., P. Schmidely, J. J. Daudin, & N. R. St-Pierre. 2008. Meta-analyses of experimental data in animal nutrition. Animal. 2:1203-1214. https://doi.org/10.1017/S1751731108002280
Scanes, C. G., & K. Pierzchala-Koziec. 2014. Biology of the gastrointestinal tract in poultry. Avian Biology Research. 7:193-222. https://doi.org/10.3184/175815514X14162292284822
Schat, K. A., B. Kaspers, & P. Kaiser. 2013. Avian Immunology. 2nd Ed. Academic Press, Boston.
Shang, Y., S. Kumar, B. Oakley, & W. K. Kim. 2018. Chicken gut microbiota: Importance and detection technology. Front. Vet. Sci. 5:524. https://doi.org/10.3389/fvets.2018.00254
Shamseer, L., D. Moher, M. Clarke, D. Ghersi, A. Liberati, M. Petticrew, P. Shekelle, & L. A. Stewart. 2015. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 349:1-25. https://doi.org/10.1136/bmj.g7647
Sharma, J. M. 2017. Avian Cellular Immunology. CRC Press, Minnesota, MN, USA. https://doi.org/10.1201/9781315137988
Silva, P. I., S. Daffre, & P. Bulet. 2000. Isolation and characterization of gomesin, an 18-residue Cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to Horseshoe crab antimicrobial peptides of the Tachyplesin family. J. Biol. Chem. 275:33464-33470. https://doi.org/10.1074/jbc.M001491200
Sholikin, M.M., Prihambodo, T.R., Qomariyah, N., Wahyudi, A.T., Jayanegara, A., Nomura, J., Nahrowi. The effect of antimicrobial peptide addition on growth performance, digestibility, small intestine morphology, and blood serum of broiler: A meta-analysis. World’s Poultry Sci. J. [Submitted].
St-Pierre, N. R. 2001. Invited review: Integrating quantitative findings from multiple studies using mixed model methodology. J. Dairy Sci. 84:741-755. https://doi.org/10.3168/jds.S0022-0302(01)74530-4
R Core Team. 2020. R : A Language and Environment for Statistical Computing. p. 1-3690.
Torki, M., D. Schokker, M. Duijster-Lensing, & M. M. Van Krimpen. 2018. Effect of nutritional interventions with quercetin, oat hulls, β-glucans, Lysozyme and fish oil on performance and health status related parameters of broilers chickens. Br. Poult. Sci. 59:579-590. https://doi.org/10.1080/00071668.2018.1496402
Tribst, A. A. L., M. A. Franchi, & M. Cristianini. 2008. Ultra-high pressure homogenization treatment combined with lysozyme for controlling Lactobacillus brevis contamination in model system. Innov. Food Sci. Emerg. Technol. 9:265-271. https://doi.org/10.1016/j.ifset.2007.07.012
Vizioli, J., P. Bulet, M. Charlet, C. Lowenberger, C. Blass, H.-M. Muller, G. Dimopoulos, J. Hoffmann, F. C. Kafatos, & A. Richman. 2000. Cloning and analysis of a cecropin gene from the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 9:75-84. https://doi.org/10.1046/j.1365-2583.2000.00164.x
Wang, D., W. Ma, R. She, Q. Sun, Y. Liu, Y. Hu, L. Liu, Y. Yang, & K. Peng. 2009. Effects of swine gut antimicrobial peptides on the intestinal mucosal immunity in specific-pathogen-free chickens. Poult. Sci. 88:967-974. https://doi.org/10.3382/ps.2008-00533
Wang, G., Q. Song, S. Huang, Y. Wang, S. Cai, H. Yu, X. Ding, X. Zeng, & J. Zhang. 2020. Effect of antimicrobial peptide Microcin J25 on growth performance, immune regulation, and intestinal microbiota in broiler chickens challenged with Escherichia coli and Salmonella. Animals. 10:345. https://doi.org/10.3390/ani10020345
Wang, R., Y. Luo, Y. Lu, D. Wang, T. Wang, W. Pu, & Y. Wang. 2019. Maggot extracts alleviate inflammation and oxidative stress in acute experimental colitis via the activation of Nrf2. Oxid. Med. Cell. Longev. 2019:1-18. https://doi.org/10.1155/2019/4703253
Wang, S., X. F. Zeng, Q. W. Wang, J. L. Zhu, Q. Peng, C. L. Hou, P. Thacker, & S. Y. Qiao. 2015. The antimicrobial peptide Sublancin ameliorates necrotic enteritis induced by Clostridium perfringens in broilers. J. Anim. Sci. 93:4750-4760. https://doi.org/10.2527/jas.2015-9284
Wang, S., X. Zeng, Q. Yang, & S. Qiao. 2016. Antimicrobial peptides as potential alternatives to antibiotics in food animal industry. Int. J. Mol. Sci. 17:603. https://doi.org/10.3390/ijms17050603
Wen, L.-F., & J.-G. He. 2012. Dose-response effects of an antimicrobial peptide, a cecropin hybrid, on growth performance, nutrient utilisation, bacterial counts in the digesta and intestinal morphology in broilers. Br. J. Nutr. 108:1756-1763. https://doi.org/10.1017/S0007114511007240
Wu, Q., J. Patočka, & K. Kuča. 2018. Insect antimicrobial peptides, a mini review. Toxins. 10:461. https://doi.org/10.3390/toxins10110461
Xiao, H., F. Shao, M. Wu, W. Ren, X. Xiong, B. Tan, & Y. Yin. 2015. The application of antimicrobial peptides as growth and health promoters for swine. J. Anim. Sci. Biotechnol. 6:19. https://doi.org/10.1186/s40104-015-0018-z
Yi, H., M. Chowdhury, Y. Huang, & X.-Q. Yu. 2014. Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98:5807-5822. https://doi.org/10.1007/s00253-014-5792-6
Yuan, W., H. T. Jin, Z. H. Ren, J. L. Deng, Z. C. Zuo, Y. Wang, H. D. Deng, & Y. T. Deng. 2015. Effects of antibacterial peptide on humoral immunity in weaned piglets. Food Agr. Immunol. 26:682-689. https://doi.org/10.1080/09540105.2015.1007448
Yue, S., J. Jie, L. Xie, Y. Li, J. Zhang, X. Lai, J. Xie, X. Guo, & Y. Zhai. 2020. Antimicrobial peptide CAMA‐syn expressed in pulmonary epithelium by recombination adenovirus inhibited the growth of intracellular bacteria. J. Gene Med. 22:0-2. https://doi.org/10.1002/jgm.3149
Zhang, G., G. F. Mathis, C. L. Hofacre, P. Yaghmaee, R. A. Holley, & T. D. Durance. 2010. Effect of a radiant energy-treated Lysozyme antimicrobial blend on the control of clostridial necrotic enteritis in broiler chickens. Avian Dis. Dig. 5: e43-e44. https://doi.org/10.1637/9549-937010-DIGEST.1
Zhang, J., L. Xie, D. Xu, S. Yue, Y. Li, X. Guo, & X. Lai. 2017. Targeting expression of antimicrobial peptide CAMA-Syn by adenovirus vector in macrophages inhibits the growth of intracellular bacteria. Gene. 630:59-67. https://doi.org/10.1016/j.gene.2017.07.079
Zhao, X., H. Wu, H. Lu, G. Li, & Q. Huang. 2013. LAMP: A database linking antimicrobial peptides. PLoS ONE. 8:e66557. https://doi.org/10.1371/journal.pone.0066557

Authors

M. M. Sholikin
A. T. Wahyudi
A. Jayanegara
anu_jayanegara@yahoo.com (Primary Contact)
J. Nomura
Nahrowi Nahrowi
Author Biography

A. Jayanegara, Department of Nutrition and Feed Technology, Faculty of Animal Science, Bogor Agricultural University

Field of interest: ruminant feed and nutrition

Email: anu_jayanegara@yahoo.com

SholikinM. M., WahyudiA. T., JayanegaraA., NomuraJ., & NahrowiN. (2021). A Meta-analysis of Antimicrobial Peptide Effects on Intestinal Bacteria, Immune Response, and Antioxidant Activity of Broilers. Tropical Animal Science Journal, 44(2), 188-197. https://doi.org/10.5398/tasj.2021.44.2.188

Article Details