Dietary supplementation with the extract from Eucommia ulmoides leaves changed epithelial restitution and gut microbial community and composition of weanling piglets


Autoři: Mijun Peng aff001;  Zhihong Wang aff001;  Sheng Peng aff002;  Minglong Zhang aff001;  Yehui Duan aff003;  Fengna Li aff003;  Shuyun Shi aff005;  Qiuling Yang aff001;  Changwei Zhang aff006
Působiště autorů: Guangdong Provincial Public Laboratory of Analysis and Testing Technology, Guangdong Institute of Analysis, Guangzhou, P. R. China aff001;  National & Local United Engineering Laboratory of Integrative Utilization Technology of , Jishou University, Zhangjiajie, P. R. China aff002;  Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Pr aff003;  Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Hunan Collaborative Innovation Center for Utilization of Botanical Functional Ingredients, Changsha, Hunan, China aff004;  College of Chemistry and Chemical Engineer, Central South University, Changsha, Hunan, China aff005;  Institute of Chemical Industry of Forest Products, CAF, Nanjing, P. R. China aff006
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223002

Souhrn

This study was conducted to compare the effects of Eucommia ulmoides leaves (EL) in different forms (EL extract, fermented EL, and EL powder) with antibiotics on growth performance, intestinal morphology, and the microbiota composition and diversity of weanling piglets. Compared to the control group, the antibiotics and EL extract significantly increased the average daily gain and decreased the feed: gain ratio as well as the diarrhea rate (P < 0.05). The EL extract significantly decreased the crypt depth and increased the ratio of villus height to crypt depth (P < 0.05), while the fermented EL group did the opposite (P < 0.05). The crypt depth in the antibiotics group was of similar value to the EL extract group, and was lower than the fermented EL and EL powder groups (P < 0.05). Compared to the control and antibiotics groups, the jejunul claudin-3 mRNA expression and the concentrations of total VFA, Chao 1, and ACE were significantly augmented in the EL extract group of piglets (P < 0.05). The EL extract groups also showed elevated Shannon (P < 0.05) and Simpson (P = 0.07) values relative to the control and antibiotics groups. At the phylum level, the EL extract group exhibited a reduced abundance of Bacteroidetes and an enhanced abundance of Firmicutes. At the genus level, the abundance of Prevotella was augmented in the EL extract group. Moreover, compared with the antibiotic group, the acetate concentration was enhanced in the EL extract and fermented EL groups. Overall, dietary supplementation with the EL extract, but not the fermented EL or EL powder, improved growth performance, jejunul morphology and function, as well as changed colonic microbial composition and diversity, which might be an alternative to confer protection against weanling stress in weanling piglets.

Klíčová slova:

Animal performance – Antibiotics – Diarrhea – Diet – Gastrointestinal tract – Microbiome – Swine – Colon


Zdroje

1. Hashemi SR, Davoodi H. Herbal plants and their derivatives as growth and health promoters in animal nutrition. Vet. Res. Commun. 2011; 35: 169–80. doi: 10.1007/s11259-010-9458-2 21213046

2. Cheng G, Hao H, Xie S, Wang X, Dai M, Huang L, et al. Antibiotic alternatives: The substitution of antibiotics in animal husbandry? Front. Microbiol. 2014; 5: 217. doi: 10.3389/fmicb.2014.00217 24860564

3. Moller FM, Bager F, Jensen NE, Madsen M, Meyling A, Wegener HC. Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. Apmis. 1998; 106: 606–22. doi: 10.1111/j.1699-0463.1998.tb01391.x 9725794

4. Stanton TB. A call for antibiotic alternatives research. Trends Microbiol. 2013; 21: 111–3. doi: 10.1016/j.tim.2012.11.002 23473628

5. Savoia D. Plant-derived antimicrobial compounds: alternatives to antibiotics. Future Microbiol. 2012; 7: 979–90. doi: 10.2217/fmb.12.68 22913356

6. Abreu AC, Mcbain AJ, Simões M. Plants as sources of new antimicrobials and resistance-modifying agents. Nat. Prod. Rep. 2012; 29: 1007–21. doi: 10.1039/c2np20035j 22786554

7. Hashemi SR, Zulkifli I, Bejo MH, Farida A. Acute toxicity study and phytochemical screening of selected herbal aqueous extract in broiler chickens. Int. J. Pharmacol. 2008; 4: 352–60. doi: 10.3923/ijp.2008.352.360

8. Shi SY, Guo KK, Tong RN, Liu YG, Tong CY, Peng MJ. Online extraction–HPLC–FRAP system for direct identification of antioxidants from solid Du-zhong brick tea. Food Chem. 2019; 288: 215–220. doi: 10.1016/j.foodchem.2019.03.013 30902284

9. Dai XP, Huang Q, Zhou BT, Gong ZC, Liu ZQ, Shi SY. Preparative isolation and purification of seven main antioxidants from Eucommia ulmoides Oliv. (Du-zhong) leaves using HSCCC guided by DPPH-HPLC experiment. Food Chem. 2013; 139: 563–570. doi: 10.1016/j.foodchem.2013.02.006 23561146

10. Yen GC, Hsieh CL. Reactive oxygen species scavenging activity of du-zhong (Eucommia ulmoides oliv.) and its active compounds. J. Agr. Food Chem. 2000; 48: 3431–6. doi: 10.1021/jf000150t 10956129

11. Zhu MQ and Sun RC. Eucommia ulmoides Oliver: A Potential Feedstock for Bioactive Products. J. Agric. Food Chem. 2018; 66: 5433−5438. doi: 10.1021/acs.jafc.8b01312 29745662

12. Zhang Q, Su Y, Zhang J. Seasonal difference in antioxidant capacity and active compounds contents of Eucommia ulmoides oliver leaf. Molecules. 2013; 18: 1857–68. doi: 10.3390/molecules18021857 23377129

13. Long C, Zhou X, Wang Q, Xie C, Li F, Fan Z, et al. Dietary supplementation of Lonicera macranthoides leaf powder improves amino acid profiles in serum and longissimus thoracis muscle of growing-finishing pigs. Anim. Nutr. 2016; 2: 271–5. doi: 10.1016/j.aninu.2016.08.006 29767115

14. Li FL, Ren AJ, Cai GH, Qu ZX, Wang ZP, Su YQ, et al. Effects of fermented Eucommia ulmoides leaves on performance, egg quality, and lipid metabolism of layers. Acta Agric. Borealioccidentalis Sinica. 2016; 28: 1137–43. http://www.en.cnki.com.cn/Article_en/CJFDTotal-XBNX201608005.htm

15. Jia ZS, Tang MC, Wu JM. The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemi. 1999; 64: 555–9. doi: 10.1016/s0308-8146(98)00102-2

16. Luo XB, Ma M, Chen B, Yao SZ, Wan ZT, Yang DJ, and Hang HW. Analysis of nine bioactive compounds in Eucommia ulmoides Oliv. and their preparation by HPLC-photodiode array detection and mass spectrometry. J. Liq. Chromatogr. Relat. Technol. 2004, 27(1): 63–81. doi: 10.1081/jlc-120027086

17. Dubois M, Gilles KA, Hamilton JK, Rebers PA, & Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 1956; 28, 350–6. doi: 10.1021/ac60111a017

18. NRC. Nutrient requirements of swine (eleventh revised edition). Washington, DC: National Academic Press; 2012. https://www.nap.edu/read/13298/chapter/1

19. Wang ZY, Duan YH, Li FN, Yang BC, Zhang JX, Hou SZ. Dietary supplementation with Lonicera macranthoides leaf powder enhances growth performance and muscle growth of Chinese Tibetan pigs. Livest. Sci. 2017; 206: 1–8. doi: 10.1016/j.livsci.2017.09.026

20. Liu YY, Li FN, Kong XF, Tan B, Li YH, Duan YH, et al. Signaling pathways related to protein synthesis and amino acid concentration in pig skeletal muscles depend on the dietary protein level, genotype and developmental stages. PLoS ONE. 2015;10: e0138277. doi: 10.1371/journal.pone.0138277 26394157

21. Kong XF, Ji YJ, Li HW, Zhu Q, Blachier F, Geng MM, et al. Colonic luminal microbiota and bacterial metabolite composition in pregnant Huanjiang mini-pigs: effects of food composition at different times of pregnancy. Sci. Rep. 2016; 6: 37224. doi: 10.1038/srep37224 27917879

22. Kong XF, Wu GY, Liao YP, Hou ZP, Liu HJ, Yin FG, et al. Effects of Chinese herbal ultra-fine powder as a dietary additive on growth performance, serum metabolites and intestinal health in early-weaned piglets. Livest. Sci. 2007; 108: 272–5. doi: 10.1016/j.livsci.2007.01.079

23. Duan YH, Tan BE, Li JJ, Liao P, Huang B, Li FN, et al. Optimal branched-chain amino acid ratio improves cell proliferation and protein metabolism of porcine enterocytesin in vivo and in vitro. Nutrition. 2018; 54: 173–81. doi: 10.1016/j.nut.2018.03.057 30048883

24. Duan Y, Li F, Tan B, Lin B, Kong X, Li Y, et al. Myokine interleukin-15 expression profile is different in suckling and weaning piglets. Anim. Nutr. 2015; 1: 30–5. doi: 10.1016/j.aninu.2015.02.005 29766983

25. Liu S, He L, Jiang Q, Duraipandiyan V, Al-Dhabi NA, Liu G, et al. Effect of dietary alpha-ketoglutarate and allicin supplementation on the cecal microbial community composition and diversity in growing pigs. J. Sci. Food Agr. 2018; https://doi.org/10.1002/jsfa.9131

26. Sun DL, Jiang X, Wu QLL, Zhou NY. Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl. Environ. Microb. 2013; 79: 5962–9. doi: 10.1128/AEM.01282-13 23872556

27. Shi Y, Leng XJ, Li XQ, Li BS, Hu B. Effect of Du-zhong (Eucommia ulmoides Oliver) leaf extract on growth, serum non-specific immune response and meat quality of crucian carp. J. Zhejiang Univ. (Agric. & Life Sci.) 2008; 34: 200–6. doi: 10.3785/j.issn.1008-9209.2008.02.013

28. Chen YM, Huang T, Song XZ, Xu LJ, Liu B, Fu YB. Effects of dietary Eucommia leaves extract on growth performance and immune function of broilers. Chin. J. Anim. Nutr. 2015; 27: 2224–30. https://www.en.cnki.com.cn/Article_en/CJFDTotal-DWYX201507029.htm

29. Caspary WF. Physiology and pathophysiology of intestinal absorption. Am. J. Clin. Nutr. 1992; 55: 299–308. doi: 10.1093/ajcn/55.1.299s 1728844

30. Pie S, Lalles JP, Blazy F, Laffitte J, Seve B, Oswald IP. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J. Nutr. 2004; 134: 641–7. doi: 10.1093/jn/134.3.641 14988461

31. Hu CH, Xiao K, Luan ZS, Song J. Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs. J. Anim. Sci. 2013; 91: 1094–101. doi: 10.2527/jas.2012-5796 23230104

32. Wang J, Li GR, Tan BE, Xiong X, Kong XF, Xiao DF, et al. Oral administration of putrescine and proline during the suckling period improves epithelial restitution after early weaning in piglets. J. Anim. Sci. 2015; 93: 1679–88. doi: 10.2527/jas.2014-8230 26020189

33. Wu SG, Tian JY, Gatesoupe FJ, Li WX, Zou H, Yang BJ, et al. Intestinal microbiota of gibel carp (Carassius auratus gibelio) and its origin as revealed by 454 pyrosequencing. World J. Microb. Biot. 2013; 29: 1585–95. doi: 10.1007/s11274-013-1322-4 23515964

34. Myer PR, Wells JE, Smith TP, Kuehn LA, Freetly HC. Cecum microbial communities from steers differing in feed efficiency. J. Anim. Sci. 2015; 93: 5327–5340. doi: 10.2527/jas.2015-9415 26641052

35. Myer PR, Smith TPL, Wells JE, Kuehn LA, Freetly HC. Rumen microbiome from steers differing in feed efficiency. PLoS ONE. 2015; 10: e0129174. doi: 10.1371/journal.pone.0129174 26030887

36. Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015; 33: 496–503. doi: 10.1016/j.tibtech.2015.06.011 26210164

37. Lange K, Buerger M, Stallmach A, Bruns T. Effects of antibiotics on gut microbiota. Digest. Dis. 2016; 34: 260–8. doi: 10.1159/000443360 27028893

38. Lin J. Antibiotic growth promoters enhance animal production by targeting intestinal bile salt hydrolase and its producers. Front. Microbiol. 2014; 5: 33. doi: 10.3389/fmicb.2014.00033 24575079

39. Feng H, Fan J, Song Z, Du X, Chen Y, Wang J, et al. Characterization and immunoenhancement activities of Eucommia ulmoides polysaccharides. Carbohyd. Polym. 2016; 136: 803–11. doi: 10.1016/j.carbpol.2015.09.079 26572415

40. Guo FC, Savelkoul HFJ, Kwakkel RP, Williams BA, Verstegen MWA. Immunoactive, medicinal properties of mushroom and herb polysaccharides and their potential use in chicken diets. Worlds Poultry Sci. J. 2003; 59: 427–40. doi: 10.1079/WPS20030026

41. Canh TT, Sutton AL, Aarnink AJ, Verstegen MW, Schrama JW, Bakker GC. Dietary carbohydrates alter the fecal composition and pH and the ammonia emission from slurry of growing pigs. J. Anim. Sci. 1998; 76: 1887–95. doi: 10.2527/1998.7671887x 9690645

42. Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, Flint HJ. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microb. 2005; 71: 3692–700. doi: 10.1128/AEM.71.7.3692–3700.2005

43. Salyers AA. Bacteroides of the human lower intestinal tract. Annu. Rev. Microbiol. 1984; 38: 293–313. doi: 10.1146/annurev.mi.38.100184.001453 6388494

44. Hong YH, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, et al. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology. 2005; 146: 5092–9. doi: 10.1210/en.2005-0545 16123168

45. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment. Pharm. Ther. 2010; 27: 104–19. doi: 10.1111/j.1365-2036.2007.03562.x 17973645

46. Macfarlane S, Macfarlane GT. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 2003; 62: 67–72. doi: 10.1079/PNS2002207 12740060

47. Thibault R, Blachier F, Darcyvrillon B, De CP, Bourreille A, Segain JP. Butyrate utilization by the colonic mucosa in inflammatory bowel diseases: a transport deficiency. Inflamm. bowel dis. 2010; 16: 684–95. doi: 10.1002/ibd.21108 19774643


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden