ORIGINAL PAPER
 
KEYWORDS
TOPICS
ABSTRACT
The present meta-analysis evaluated the effect of the level of antimicrobial peptides (AMPs) on broiler chicken growth performance, digestibility, small intestine morphology and blood serum parameters. The database was developed from 29 articles comprising 36 experiments. Data were analyzed using a mixed model methodology considering the levels of AMPs as fixed effects and different studies as random effects. It was shown that an increased AMPs addition level quadratically influenced body weight (BW), average daily gain (ADG) and feed conversion ratio (FCR) (P < 0.05). Simultaneously, it linearly reduced mortality (P < 0.05) both in the starter and finisher periods. There was a linear increase in metabolizable energy (P < 0.05). Small intestine morphology in the duodenum, as indicated by villus height and villus height to crypt depth ratio linearly increased, while the crypt depth was linearly decreased (P < 0.05). The mucosa thickness was quadratically affected in the jejunum, while the crypt depth linearly decreased (P < 0.05). Categorical analysis showed that AMPs had a comparable effect with antibiotics on broiler performance (BW, ADG, FCR) (P > 0.05); a similar improvement was shown in the control group (P < 0.01). In conclusion, it is evidenced that AMPs can be used as an effective replacer of antibiotic growth promoters (AGP) because they can improve growth performance, digestibility, small intestine morphology and blood serum parameters of broiler in all rearing periods. Also, the optimal doses of dietary AMPs addition at 337 and 359 mg/kg of diet for the starter and finisher phases, respectively, are suggested.
ACKNOWLEDGEMENTS
This study was fully funded by the Ministry of Education and Culture, the Republic of Indonesia, through the scholarship research scheme, namely ‘Master Education Towards Doctor for Excellent Bachelor (PMDSU)’ grant no. 2136/IT3.L1 PN/2021 in the 2021 fiscal year. This paper was also a part of the sandwich-like program (PKPI) grand number T/2134/D3.2/Kd.02.00/2019 at Chiba University, Japan in 2019.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
REFERENCES (62)
1.
Abdel-Latif M.A., El-Far A.H., Elbestawy A.R., Ghanem R., Mousa S.A., Abd El-Hamid H.S., 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, e0185153, http://doi.org/10.1371/journal....
 
2.
Aguirre A.T.A., Acda S.P., Angeles A.A., Oliveros M.C.R., Merca F.E., Cruz F.A., 2015. Effect of bovine lactoferrin on growth performance and intestinal histologic features of broilers. Philipp. J. Vet. Anim. Sci. 41, 12–20.
 
3.
Ali A.H.H., Mohanny K.M., 2014. Effect of injection with bee venom extract on productive performance and immune response of broiler chicks. J. Anim. Poult. Prod. 5, 237–246, https://doi.org/10.21608/jappm....
 
4.
Aliakbarpour H.R., Chamani M., Rahimi G., Sadeghi A.A., Qujeq D., 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, http://doi.org/10.5713/ajas.20....
 
5.
Bai J., Wang R., Yan L., Feng J., 2019. Co-supplementation of dietary seaweed powder and antibacterial peptides improves broiler growth performance and immune function. Braz. J. Poult. Sci. 21, eRBCA-2018-0826, https://doi.org/10.1590/1806-9....
 
6.
Bao H., She R., Liu T. et al., 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.200....
 
7.
Bauer E., Jakob S., Mosenthin R., 2005. Principles of physiology of lipid digestion. Asian-Australas. J. Anim. Sci. 18, 282–295, https://doi.org/10.5713/ajas.2....
 
8.
Choi S.C., Ingale S.L., Kim J.S., Park Y.K., Kwon I.K., Chae B.J., 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/10.1080/000716....
 
9.
Choi S.C., Ingale S.L., Kim J.S., Park Y.K., Kwon I.K., Chae B.J., 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.anif....
 
10.
Daneshmand A., Kermanshahi H., Sekhavati M.H., Javadmanesh A., Ahmadian M., 2019. 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....
 
11.
Daneshmand A., Kermanshahi H., Sekhavati M.H., Javadmanesh A., Ahmadian M., Alizadeh M., Aldavoodi A., 2020. Effects of cLFchimera on intestinal morphology, integrity, microbiota, and immune cells in broiler chickens challenged with necrotic enteritis. Sci. Rep. 10, 17704, https://doi.org/10.1038/s41598....
 
12.
EFSA (European Food Safety Authority), Bronzwaer S., Kass G., Robinson T., Tarazona J., Verhagen H., Verloo D., Vrbos D., Hugas M., 2019. Editorial on food safety regulatory research needs 2030. EFSA J. 17, e170622, https://doi.org/10.2903/j.efsa....
 
13.
Enany M., El Gammal A.E.A., Solimane R., El Sissi A., Hebashy A., 2017. Evaluation of lactoferrin immunomodulatory effect on the immune response of broiler chickens. Suez Canal Vet. Med. J. 22, 135–146, https://doi.org/10.21608/scvmj....
 
14.
Feingold K.R., Grunfeld C., 2000. Introduction to lipids and lipoproteins. In: Endotext. MDText.com, Inc., South Dartmouth, MA (USA).
 
15.
Geier M.S., Torok V.A., Guo P., Allison G.E., Boulianne M., Janardhana V., Bean A.G.D., Hughes R.J., 2011. The effects of lactoferrin on the intestinal environment of broiler chickens. Br. Poult. Sci. 52, 564–572, https://doi.org/10.1080/000716....
 
16.
Gong M., Anderson D., Rathgeber B., MacIsaac J., 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/p....
 
17.
Han S.M., Lee K.G., Yeo J.H., Oh B.Y., Kim B.S., Lee W., Baek H.J., Kim S.T., Hwang S.J., Pak S.C., 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.201....
 
18.
Hu X.F., Guo Y.M., Huang B.Y., Bun S., Zhang L.B., Li J.H., Liu D., Long F.Y., Yang X., Jiao P., 2010. The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrient transporter expression of stressed broiler chickens. Poult. Sci. 89, 1967–1974, https://doi.org/10.3382/ps.200....
 
19.
Irawan A., Hidayat C., Jayanegara A., Ratriyanto A., 2020. Essential oils as growth-promoting additives on performance, nutrient digestibility, cecal microbes, and serum metabolites of broiler chickens: a meta-analysis. Asian-Australas. J. Anim. Sci. https://doi.org/10.5713/ab.20.....
 
20.
Irawan A., Sofyan A., Ridwan R., Hassim H.A., Respati A.N., Wardani W.W., Sadarman, Astuti W.D., Jayanegara A., 2021. Effects of different lactic acid bacteria groups and fibrolytic enzymes as additives on silage quality: a meta-analysis. Bioresour. Technol. Rep. 14, 100654, https://doi.org/10.1016/j.bite....
 
21.
Jiang Y.B., Yin Q.Q., Yang Y.R., 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....
 
22.
Jin Z., Yang Y.X., Choi J.Y. et al., 2008. Effects of potato (Solanum tuberosum L. cv. Golden valley) protein having antimicrobial activity on the growth performance, and intestinal microflora and morphology in weanling pigs. Anim. Feed Sci. Technol. 140, 139–154, https://doi.org/10.1016/j.anif....
 
23.
Józefiak A., Engberg R.M., 2017. Insect proteins as a potential source of antimicrobial peptides in livestock production. a review. J. Anim. Feed Sci. 26, 87–99, https://doi.org/10.22358/jafs/....
 
24.
Karimzadeh S., Rezaei M., Teimouri Yansari A., 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, https://doi.org/10.22069/psj.2....
 
25.
Karimzadeh S., Rezaei M., Teimouri-Yansari A., 2017a. Effect of canola peptides, antibiotic, probiotic and prebiotic on performance, digestive enzymes activity and some ileal aerobic bacteria in broiler chicks. Iran J. Anim. Sci. 48, 129–139, https://doi.org/10.22059/ijas.....
 
26.
Karimzadeh S., Rezaei M., Yansari A.T., 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.livs....
 
27.
Kierończyk B., Rawski M., Mikołajczak Z., Świątkiewicz S., Józefiak D., 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/ani100....
 
28.
Kim D.H., Han S.M., Keum M.C., Lee S., An B.K., Lee S.-R., Lee K.-W., 2018. Evaluation of bee venom as a novel feed additive in fast-growing broilers. Br. Poult. Sci. 59, 435–442, https://doi.org/10.1080/000716....
 
29.
Leeson S., Summers J.D., 2009. Commercial Poultry Nutrition. Nottingham University Press. Nottingham (UK), https://doi.org/10.7313/UPO978...
 
30.
Li Z., Mao R., Teng D., Hao Y., Chen H., Wang X., Wang X., Yang N., Wang J., 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....
 
31.
Liu D., Guo Y., Wang Z., Yuan J., 2010. Exogenous lysozyme influences Clostridium perfringens colonization and intestinal barrier function in broiler chickens. Avian Pathol. 39, 17–24, https://doi.org/10.1080/030794....
 
32.
Ma J.L., Zhao L.H., Sun D.D., Zhang J., Guo Y.P., Zhang Z.Q., Ma Q.G., Ji C., Zhao L.H., 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....
 
33.
Magana M., Pushpanathan M., Santos A.L. et al., 2020. The value of antimicrobial peptides in the age of resistance. Lancet Infect. Dis. 20, E216–E230, https://doi.org/10.1016/S1473-....
 
34.
Ohh S.H., Shinde P.L., Jin Z., Choi J.Y., Hahn T.-W., Lim H.T., Kim G.Y., Park Y., Hahm K.-S., Chae B.J., 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.200....
 
35.
Pinheiro J., Bates D., DebRoy S. et al., 2020. nlme: Linear and Nonlinear Mixed Effects Models, https://cran.r-project.org/web....
 
36.
Prihambodo T., Sholikin M.M., Qomariyah N., et al., 2021. Effects of dietary flavonoids on performance, blood constituents, carcass composition and small intestinal morphology of broilers: a meta-analysis. Anim. Biosci. 34, 434–442, https://doi.org/10.5713/ajas.2....
 
37.
R Core Team, 2020. R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna (Austria), http://www.r-project.org/index....
 
38.
Saks V.A., Ventura-Clapier, R. (Editors), 1994. Cellular Bioenergetics: Role of Coupled Creatine Kinases. Springer Science+Business Media. Dordrecht (the Netherlands), https://doi.org/10.1007/978-1-....
 
39.
Salavati M.E., Rezaeipour V., Abdullahpour R., Mousavi N., 2020. 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....
 
40.
Sauvant D., Schmidely P., Daudin J.J., St-Pierre N.R., 2008. Meta-analyses of experimental data in animal nutrition. Animal 2, 1203–1214, https://doi.org/10.1017/s17517....
 
41.
Selle P.H., Ravindran V., Ravindran G., Bryden W.L., 2007. Effects of dietary lysine and microbial phytase on growth performance and nutrient utilisation of broiler chickens. Asian-Australas. J. Anim. Sci. 20, 1100–1107, https://doi.org/10.5713/ajas.2....
 
42.
Skosyrev V.S., Kulesskiy E.A., Yakhnin A.V., Temirov Y.V., Vinokurov L.M., 2003. Expression of the recombinant antibacterial peptide sarcotoxin IA in Escherichia coli cells. Protein Expr. Purif. 28, 350–356, https://doi.org/10.1016/s1046-....
 
43.
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.s0....
 
44.
Svihus B., 2014. Function of the digestive system. J. Appl. Poult. Res. 23, 306–314, https://doi.org/10.3382/japr.2....
 
45.
Tanhaeian A., Mirzaii M., Pirkhezranian Z., Sekhavati M.H., 2020. Generation of an engineered food-grade Lactococcus lactis strain for production of an antimicrobial peptide: in vitro and in silico evaluation. BMC Biotechnol. 20, 19, https://doi.org/10.1186/s12896....
 
46.
Tanhaiean A., Azghandi M., Razmyar J., Mohammadi E., Sekhavati M.H., 2018a. Recombinant production of a chimeric antimicrobial peptide in E. coli and assessment of its activity against some avian clinically isolated pathogens. Microb. Pathog. 122, 73–78, https://doi.org/10.1016/j.micp....
 
47.
Tanhaieian A., Sekhavati M.H., Ahmadi F.S., Mamarabadi M., 2018b. Heterologous expression of a broad-spectrum chimeric antimicrobial peptide in Lactococcus lactis: Its safety and molecular modeling evaluation. Microb. Pathog. 125, 51–59, https://doi.org/10.1016/j.micp....
 
48.
Torki M., Schokker D., Duijster-Lensing M., Van Krimpen M.M., 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/10.1080/000716....
 
49.
Vanrolleghem W., Tanghe S., Verstringe S., Bruggeman G., Papadopoulos D., Trevisi P., Zentek J., Sarrazin S., Dewulf J., 2019. Potential dietary feed additives with antibacterial effects and their impact on performance of weaned piglets: a meta-analysis. Vet. J. 249, 24–32, http://doi.org/10.1016/j.tvjl.....
 
50.
Wang D., Ma W., She R., Sun Q., Liu Y., Hu Y., Liu L., Yang Y., Peng K., 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.200....
 
51.
Wang S., Zeng X.F., Wang Q.W., et al., 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.20....
 
52.
Wang G., Song Q., Huang S., Wang Y., Cai S., Yu H., Ding X., Zeng X., Zhang J., 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/ani100....
 
53.
Wang S., Zeng X., Yang Q., Qiao S., 2016. Antimicrobial peptides as potential alternatives to antibiotics in food animal industry. Int. J. Mol. Sci. 17, 603, https://doi.org/10.3390/ijms17....
 
54.
Wang Y., Shan T., Xu Z., Liu J., Feng J., 2006. Effect of lactoferrin on the growth performance, intestinal morphology, and expression of PR-39 and protegrin-1 genes in weaned piglets. J. Anim. Sci. 84, 2636–2641, https://doi.org/10.2527/jas.20....
 
55.
Wen L.-F., He J.-G., 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/S00071....
 
56.
Xiao H., Shao F., Wu M., Ren W., Xiong X., Tan B., Yin Y., 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....
 
57.
Xiao H., Tan B.E., Wu M.M., Lin Y.L., Li T.J., Yuan D.X, and Li L., 2013. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: II. Intestinal morphology and function. J. Anim. Sci. 91, 4750–4756, https://doi.org/10.2527/jas.20....
 
58.
Xu B., Fu J., Zhu L., Li Z., Jin M., Wang Y., 2021. Overall assessment of antibiotic substitutes for pigs: a set of meta-analyses. J. Anim. Sci. Biotechnol. 12, 3, http://doi.org/10.1186/s40104-....
 
59.
Yi H.-Y., Chowdhury M., Huang Y.-D., Yu X.-Q., 2014. Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98, 5807–5822, https://doi.org/10.1007/s00253....
 
60.
Yoon J.H., Ingale S.L., Kim J.S., Kim K.H., Lohakare J., Park Y.K., Park J.C., Kwon I.K., Chae B.J., 2013. Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J. Sci. Food Agric. 93, 587–592, https://doi.org/10.1002/jsfa.5....
 
61.
Zhang G., Mathis G.F., Hofacre C.L., Yaghmaee P., Holley R.A., Duranc T.D., 2010. Effect of a radiant energy-treated lysozyme antimicrobial blend on the control of clostridial necrotic enteritis in broiler chickens. Avian Dis. 54, 1298–1300, https://doi.org/10.1637/9370-0....
 
62.
Zhao X., Wu H., Lu H., Li G., Huang Q., 2013. LAMP: a database linking antimicrobial peptides. PLoS ONE 8, e66557, https://doi.org/10.1371/journa....
 
 
CITATIONS (10):
1.
Changes in nutritional and antinutritional aspects of soybean meals by mechanical and solid-state fermentation treatments with Bacillus subtilis and Aspergillus oryzae
Wara Suprayogi, Adi Ratriyanto, Novi Akhirini, Rendi Hadi, Wahyu Setyono, Agung Irawan
Bioresource Technology Reports
 
2.
Antimicrobial peptides from freshwater invertebrate species: potential for future applications
Robert Egessa
Molecular Biology Reports
 
3.
Effects of sesame meal bioactive peptides, individually or in combination with a mixture of essential oils, on growth performance, carcass, jejunal morphology, and microbial composition of broiler chickens
Mohammad Bahadori, Vahid Rezaeipour, Rohullah Abdullahpour, Mehrdad Irani
Tropical Animal Health and Production
 
4.
A meta-analysis of the effects of clay mineral supplementation on alkaline phosphatase, broiler health, and performance
Mohammad Sholikin, Sadarman, Agung Irawan, Ahmad Sofyan, Anuraga Jayanegara, Barlah Rumhayati, Cecep Hidayat, Danung Adli, Hardi Julendra, Hendra Herdian, Ifa Manzila, Mohammad Hudaya, Muhammad Harahap, Novia Qomariyah, Rahmat Budiarto, Rantan Krisnan, Santiananda Asmarasari, Sari Hayanti, Teguh Wahyono, Tri Priyatno, Tri Ujilestari, Windu Negara, Wulandari, Nahrowi
Poultry Science
 
5.
Pengaruh Pola Pemberian Nutrisi Terhadap Pertumbuhan Anak Ayam Broiler di Kecamatan Tembung, Kota Medan
Febry Rahmadhani Hasibuan, Putri Agustina Anggraini Arwira, Raini Dahriana Pulungan, Adyla Syukhraini Marwi, Aziz Husein Nasution
Jurnal Biologi
 
6.
A meta-analysis: Protein level of the substrate affect nutrient, macromineral, and amino acid profiles of maggot
Ki Ageng Sarwono, Rakhmad Perkasa Harahap, Pamungkas Rizki Ferdian, Avry Pribadi, Eyet Mulyati, Herman Sari, Heru Ponco Wardono, Lincah Andadari, Retno Agustarini, Rusli Fidriyanto, Septiantina Dyah Riendriasari, Tri Hadi Handayani, Yetti Heryati, Novia Qomariyah, Mohammad Miftakhus Sholikin
IOP Conference Series: Earth and Environmental Science
 
7.
Effects of antibacterial peptide microcin J25 on growth performance, antioxidant capacity, intestinal barrier function and intestinal microbiota in pigeon squabs
Heng Cao, Yinglin Lu, Xingyu Zhang, Jing Zhou, Fan Li, Zaixu Pan, Shanjin Xu, Minli Yu
Italian Journal of Animal Science
 
8.
Vitamin C variation in citrus in response to genotypes, storage temperatures, and storage times: A systematic review and meta-analysis
Rahmat Budiarto, Syariful Mubarok, Mohammad Miftakhus Sholikin, Dwi Novanda Sari, Ana Khalisha, Stefina Liana Sari, Bayu Pradana Nur Rahmat, Tri Ujilestari, Danung Nur Adli
Heliyon
 
9.
Investigating the impact of storage duration and temperature on vitamin C in various citrus genotypes: A meta-analysis method
Rahmat Budiarto, Danung Nur Adli, Teguh Wahyono, Tri Ujilestari, Mohammad Miftakhus Sholikin, Syariful Mubarok, Dwi Novanda Sari, Ana Khalisha, Stefina Liana Sari, Supatida Abdullakasim
MethodsX
 
10.
Examining performance, milk, and meat in ruminants fed with macroalgae and microalgae: A meta-analysis perspective
Muhammad Ainsyar Harahap, Slamet Widodo, Ulvi Fitri Handayani, Ririen Indriawaty Altandjung, Wulandari, Awistaros Angger Sakti, Bayu Andri Atmoko, Windu Negara, Yelsi Listiana Dewi, Hardi Julendra, Ahmad Sofyan, Tegoh Wahyono, Tri Ujilestari, Bilal Ahmed, Novia Qomariyah, Mohammad Miftakhus Sholikin, Zein Ahmad Baihaqi
Tropical Animal Health and Production
 
ISSN:1230-1388
Journals System - logo
Scroll to top