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Overall assessment of antimicrobial peptides in piglets: a set of meta-analyses

Published online by Cambridge University Press:  08 July 2020

B. C. Xu ,
J. Fu ,
L. Y. Zhu ,
Z. Li ,
Y. Z. Wang  and
M. L. Jin Open the ORCID record for M. L. Jin [Opens in a new window]
B. C. Xu
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
J. Fu
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
L. Y. Zhu
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
Z. Li
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
Y. Z. Wang
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
M. L. Jin*
Affiliation:
Key laboratory of Molecular Animal Nutrition, Ministry of Education, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed, Ministry of Agriculture, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China National Engineering Laboratory of Biological Feed Safety and Pollution Prevention and Control, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Key Laboratory of Animal Nutrition and Feed Science of Zhejiang Province, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China Institute of Feed Science, College of Animal Science, Zhejiang University, 866 Yuhang Tang Road, Hangzhou, Zhejiang310058, P.R. China
*
†E-mail: [email protected]
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Abstract

Developing alternatives to antibiotics is an urgent need in livestock production. Antimicrobial peptides (AMPs) are regarded as powerful antibiotic substitutes (ASs) because AMPs have broad-spectrum antimicrobial activities and growth-promoting ability. Here, we aimed to comprehensively assess the effects of AMPs on the growth performance, diarrhea rate, intestinal morphology and immunity of healthy or challenged piglets, compared with an antibiotics group or negative control group. We performed a set of meta-analyses of feeding trials from database inception to 27 May 2019. Among the 1379 identified studies, 20 were included in our meta-analyses (56 arms and 4067 piglets). The meta-analyses revealed that (1) compared with the negative control group, AMPs significantly improved the healthy piglets’ average daily gain (ADG), average daily feed intake (ADFI), gain : feed ratio (G/F), levels of immune globulin (Ig) IgM and IgG, and intestinal villus height : crypt depth ratio (V/C) (P < 0.05). Meanwhile, AMPs significantly increased the challenged piglets’ ADG, ADFI, G/F and V/C of the jejunum and ileum, and notably deceased the diarrhea rate (P < 0.05); (2) compared with antibiotics group, the effects of AMPs were slightly weaker than those of antibiotics in the healthy piglets, but AMPs have similar effects to those of antibiotics in challenged piglets. In a higher purity, the optimal dose of AMPs may be approximately 0.01%. Our findings indicate that AMPs can improve piglet growth performance, enhance immunity, benefit intestinal morphology and decrease the diarrheal rate. AMPs could be great ASs especially under infection conditions.

Keywords

antimicrobial peptidesantibiotic substitutemeta-analysispigbacteria challenge
Type
Research Article
Information
animal , Volume 14 , Issue 12 , December 2020 , pp. 2463 - 2471
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of The Animal Consortium

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References

Chou, S, Wang, J, Shang, L, Akhtar, MU, Wang, Z, Shi, B, Feng, X and Shan, A 2019. Short, symmetric-helical peptides have narrow-spectrum activity with low resistance potential and high selectivity. Biomaterials Science 7, 2394–2409.CrossRefGoogle ScholarPubMed
Cutler, SA, Lonergan, SM, Cornick, N, Johnson, AK and Stahl, CH 2007. Dietary inclusion of colicin E1 is effective in preventing postweaning diarrhea caused by F18-positive Escherichia coli in pigs. Antimicrobial Agents and Chemotherapy 51, 3830–3835.CrossRefGoogle ScholarPubMed
Eng, C, Kramer, CK, Zinman, B and Retnakaran, R 2014. Glucagon-like peptide-1 receptor agonist and basal insulin combination treatment for the management of type 2 diabetes: a systematic review and meta-analysis. Lancet 384, 2228–2234.CrossRefGoogle ScholarPubMed
Groschwitz, KR and Hogan, SP 2009. Intestinal barrier function: molecular regulation and disease pathogenesis. Journal of Allergy and Clinical Immunology 124, 21–22.Google ScholarPubMed
Higgins, JP and Thompson, SG 2002. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 1539–1558.CrossRefGoogle Scholar
Hu, P, Zhao, F, Zhu, W and Wang, J 2019. Effects of early-life lactoferrin intervention on growth performance, small intestinal function and gut microbiota in suckling piglets. Food & Function 10, 5361–5373.CrossRefGoogle ScholarPubMed
Li, Z, Liu, H, Xu, B and Wang, Y 2019. Enterotoxigenic Escherichia coli interferes fatp4-dependent long-chain fatty acid uptake of intestinal epithelial enterocytes via phosphorylation of ERK1/2-PPARgamma pathway. Frontiers in Physiology 10, 798.CrossRefGoogle ScholarPubMed
Liu, H, Cao, X, Wang, H, Zhao, J, Wang, X and Wang, Y 2019. Antimicrobial peptide KR-32 alleviates Escherichia coli K88-induced fatty acid malabsorption by improving expression of fatty acid transporter protein 4 (FATP4). Journal of Animal Science 97, 2342–2356.CrossRefGoogle Scholar
Marshall, BM and Levy, SB 2011. Food animals and antimicrobials impacts on human health. Clinical Microbiology Reviews 24, 718–733.CrossRefGoogle ScholarPubMed
Ministry of Agriculture and Rural Affairs of the People’s Republic of China 2018. Notice of the ministry of agriculture and rural affairs office on the pilot work on the reduction of the use of veterinary antimicrobial drugs. Retrieved on 27 May 2019 from http://www.moa.gov.cn/govpublic/SYJ/201804/t20180420_6140711.htmGoogle Scholar
Moher, D, Liberati, A and Tetzlaff, J 2009. Altman DG and The PRISMA Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. GroupPLoS Medicine 6, e1000097.Google ScholarPubMed
Peng, Z, Wang, A, Xie, L, Song, W, Wang, J, Yin, Z, Zhou, D and Li, F 2016. Use of recombinant porcine β-defensin 2 as a medicated feed additive for weaned piglets. Scientific Reports 6, 26790.CrossRefGoogle ScholarPubMed
Peterson, LW and Artis, D 2014. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nature Reviews Immunology 14, 141–153.CrossRefGoogle ScholarPubMed
Review on Antimicrobial Resistance 2014. Tackling a crisis for the health and wealth of nations. Retrieved on 27 May 2019 from https://amr-review.org/Google Scholar
Shan, T, Wang, Y, Wang, Y, Liu, J and Xu, Z 2007. Effect of dietary lactoferrin on the immune functions and serum iron level of weanling piglets. Journal of Animal Science 85, 2140–2146.CrossRefGoogle ScholarPubMed
Tang, ZR, Deng, H, Zhang, XL and Zen, Y 2013. Effects of orally administering the antimicrobial peptide buforin II on small intestinal mucosal membrane integrity, the expression of tight junction proteins and protective factors in weaned piglets challenged by enterotoxigenic Escherichia coli. Animal Feed Science and Technology 186, 177–185.CrossRefGoogle Scholar
Tang, X, Fatufe, AA, Yin, Y, Tang, Z, Wang, S, Liu, Z, Xinwu, and Li, TJ 2012. Dietary supplementation with recombinant lactoferrampin-lactoferricin improves growth performance and affects serum parameters in piglets. Journal of Animal and Veterinary Advances 11, 2548–2555.Google Scholar
Tang, Z, Xu, L, Shi, B, Deng, H, Lai, X, Liu, J and Sun, Z 2016. Oral administration of synthetic porcine beta-defensin-2 improves growth performance and cecal microbial flora and down-regulates the expression of intestinal toll-like receptor-4 and inflammatory cytokines in weaned piglets challenged with enter. Animal Science Journal 87, 1258–1266.CrossRefGoogle Scholar
Tang, Z, Yin, Y, Zhang, Y, Huang, R, Sun, Z, Li, T, Chu, W, Kong, X, Li, L, Geng, M and Tu, Q 2009. Effects of dietary supplementation with an expressed fusion peptide bovine lactoferricin-lactoferrampin on performance, immune function and intestinal mucosal morphology in piglets weaned at age 21 d. British Journal of Nutrition 101, 998–1005.CrossRefGoogle ScholarPubMed
US Food and Drug Administration 2018. Summary report on antimicrobials sold or distributed for use in food-producing animals. Retrieved on 27 May 2019 from https://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM628538.pdfGoogle Scholar
Van Boeckel, TP, Pires, J, Silvester, R, Zhao, C, Song, J, Criscuolo, NG, Gilbert, M, Bonhoeffer, S and Laxminarayan, R 2019. Global trends in antimicrobial resistance in animals in low- and middle-income countries. Science 365, 6459.CrossRefGoogle ScholarPubMed
Wan, J, Li, Y, Chen, D, Yu, B, Chen, G, Zheng, P, Mao, X, Yu, J and He, J 2016. Recombinant plectasin elicits similar improvements in the performance and intestinal mucosa growth and activity in weaned pigs as an antibiotic. Animal Feed Science and Technology 211, 216–226.CrossRefGoogle Scholar
Wang, J, Dou, X, Song, J, Lyu, Y, Zhu, X, Xu, L, Li, W and Shan, A 2019. Antimicrobial peptides: promising alternatives in the post feeding antibiotic era. Medicinal Research Reviews 39, 831–859.CrossRefGoogle ScholarPubMed
Wang, Y, Shan, T, Xu, Z, Liu, J and Feng, J 2006. Effect of lactoferrin on the growth performance, intestinal morphology, and expression of PR-39 and protegrin-1 genes in weaned piglets. Journal of Animal Science 84, 2636–2641.CrossRefGoogle ScholarPubMed
Wu, S, Zhang, F, Huang, Z, Liu, H, Xie, C, Zhang, J, Thacker, PA and Qiao, S 2012. Effects of the antimicrobial peptide cecropin AD on performance and intestinal health in weaned piglets challenged with Escherichia coli. Peptides 35, 255–230.CrossRefGoogle ScholarPubMed
Xiao, H, Tan, BE, Wu, MM, Yin, YL, Li, TJ, Yuan, DX and Li, L 2013a. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: II. Intestinal morphology and function. Journal of Animal Science 91, 4750–4756.CrossRefGoogle ScholarPubMed
Xiao, H, Wu, MM, Tan, BE, Yin, YL, Li, TJ, Xiao, DF and Li, L 2013b. Effects of composite antimicrobial peptides in weanling piglets challenged with deoxynivalenol: I. Growth performance, immune function, and antioxidation capacity. Journal of Animal Science 91, 4772–4780.CrossRefGoogle ScholarPubMed
Xiong, X, Yang, HS, Li, L, Wang, YF, Huang, RL, Li, FN, Wang, SP and Qiu, W 2014. Effects of antimicrobial peptides in nursery diets on growth performance of pigs reared on five different farms. Livestock Science 167, 206–210.CrossRefGoogle Scholar
Xu, B, Zhu, L, Fu, J, Li, Z, Wang, Y and Jin, M 2019. Overall assessment of fermented feed for pigs: a series of meta-analyses. Journal of Animal Science 97, 4810–4821.CrossRefGoogle ScholarPubMed
Xu, B, Li, Z, Wang, C, Fu, J, Zhang, Y, Wang, Y and Lu, Z 2020. Effects of fermented feed supplementation on pig growth performance: a meta-analysis. Animal Feed Science and Technology 259, 114315.CrossRefGoogle Scholar
Yeaman, MR and Yount, NY 2003. Mechanisms of antimicrobial peptide action and resistance. Pharmacological Reviews 55, 27–55.CrossRefGoogle ScholarPubMed
Yi, H, Zhang, L, Gan, Z, Xiong, H, Yu, C, Du, H and Wang, Y 2016. High therapeutic efficacy of Cathelicidin-WA against postweaning diarrhea via inhibiting inflammation and enhancing epithelial barrier in the intestine. Scientific Reports 6, 25679.CrossRefGoogle ScholarPubMed
Yoon, JH, Ingale, SL, Kim, JS, Kim, KH, Lee, SH, Park, YK, Kwon, IK and Chae, BJ 2012. Effects of dietary supplementation of antimicrobial peptide-A3 on growth performance, nutrient digestibility, intestinal and fecal microflora and intestinal morphology in weanling pigs. Animal Feed Science & Technology 177, 98–107.CrossRefGoogle Scholar
Yoon, JH, Ingale, SL, Kim, JS, Kim, KH, Lohakare, J, Park, YK, Park, JC, Kwon, IK and Chae, BJ 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. Journal of the Science of Food and Agriculture 93, 587–592.Google ScholarPubMed
Yoon, JH, Ingale, SL, Kim, JS, Kim, KH, Lee, SH, Park, YK, Lee, SC, Kwon, IK and Chae, BJ 2014. Effects of dietary supplementation of synthetic antimicrobial peptide-A3 and P5 on growth performance, apparent total tract digestibility of nutrients, fecal and intestinal microflora and intestinal morphology in weanling pigs. Livestock Science 159, 53–60.CrossRefGoogle Scholar
Zhang, H, Zhang, B, Zhang, X, Wang, X, Wu, K and Guan, Q 2017. Effects of cathelicidin-derived peptide from reptiles on lipopolysaccharide-induced intestinal inflammation in weaned piglets. Veterinary Immunology and Immunopathology 192, 41–53.CrossRefGoogle ScholarPubMed
Zhou, Z, Huang, J, Hao, H, Wei, H, Zhou, Y and Peng, J 2019. Applications of new functions for inducing host defense peptides and synergy sterilization of medium chain fatty acids in substituting in-feed antibiotics. Journal of Functional Foods 52, 348–359.CrossRefGoogle Scholar