Effects of anti-inflammatory and digestive-promoting fermented Chinese herbs on cecum microbiota composition and content metabolome of Chinese chickens (Gallus domesticus)

References

• Ansaldo E, Slayden LC, Ching KL, Koch MA, Wolf NK, Plichta DR, Brown EM, Graham DB, Xavier RJ, Moon JJ, et al. 2019. Akkermansia muciniphila induces intestinal adaptive immune responses during homeostasis. Science. 364(6446):1179–1184. doi: 10.1126/science.aaw7479.
   PubMed Web of Science ®Google Scholar
• Artdita CA, Zhuang YR, Liu TY, Cheng CY, Hsiao FSH, Lin YY. 2021. The effect of feeding restriction on the microbiota and metabolome response in late-phase laying hens. Animals. 11(11):3043. doi: 10.3390/ani11113043.
   Web of Science ®Google Scholar
• Bortoluzzi C, Rochell SJ, Applegate TJ. 2018. Threonine, arginine, and glutamine: influences on intestinal physiology, immunology, and microbiology in broilers. Poult Sci. 97(3):937–945. doi: 10.3382/ps/pex394.
   PubMed Web of Science ®Google Scholar
• Bortoluzzi C, Fernandes JIM, Doranalli K, Applegate TJ. 2020. Effects of dietary amino acids in ameliorating intestinal function during enteric challenges in broiler chickens. Anim. Feed Sci. Technol. 262:114383. doi: 10.1016/j.anifeedsci.2019.114383.
   Web of Science ®Google Scholar
• Boz H. 2015. Ferulic acid in cereals - A review. Czech J Food Sci. 33(1):1–7. doi: 10.17221/401/2014-CJFS.
   Web of Science ®Google Scholar
• Bu F, Zhang S, Duan Z, Ding Y, Chen T, Wang R, Feng Z, Shi G, Zhou J, Chen Y. 2020. A critical review on the relationship of herbal medicine, Akkermansia muciniphila, and human health. Biomed Pharmacother. 128:110352. doi: 10.1016/j.biopha.2020.110352.
   PubMed Web of Science ®Google Scholar
• Caekebeke N, Ringenier M, De Meyer F, Ducatelle R, Ongena N, Van Immerseel F, Dewulf J. 2020. A study on risk factors for macroscopic gut abnormalities in intensively reared broiler chickens. Avian Pathol. 49(2):193–201. doi: 10.1080/03079457.2019.1711019.
   PubMed Web of Science ®Google Scholar
• Cani PD, de Vos WM. 2017. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 8:1765. doi: 10.3389/fmicb.2017.01765.
   PubMed Web of Science ®Google Scholar
• Cui W, Cui H, Peng X, Fang J, Zuo Z, Liu X, Wu B. 2011. Changes of relative weight and cell cycle, and lesions of bursa of Fabricius induced by dietary excess vanadium of broilers. Biol Trace Elem Res. 143(1):251–260. doi: 10.1007/s12011-010-8832-9.
   PubMed Web of Science ®Google Scholar
• Derrien M, Belzer C, de Vos WM. 2017. Akkermansiamuciniphila and its role in regulating host functions. Microb Pathog. 106:171–181. doi: 10.1016/j.micpath.2016.02.005.
   PubMed Web of Science ®Google Scholar
• Dixon P. 2003. VEGAN, a package of R functions for community ecology. J Vegetation Science. 14(6):927–930. doi: 10.1111/j.1654-1103.2003.tb02228.x.
   Web of Science ®Google Scholar
• Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 10(10):996–998. doi: 10.1038/nmeth.2604.
   PubMed Web of Science ®Google Scholar
• Ferri M, Ranucci E, Romagnoli P, Giaccone V. 2017. Antimicrobial resistance: a global emerging threat to public health systems. Crit Rev Food Sci Nutr. 57(13):2857–2876. doi: 10.1080/10408398.2015.1077192.
   PubMed Web of Science ®Google Scholar
• Ganesh BP, Klopfleisch R, Loh G, Blaut M. 2013. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium-infected gnotobiotic mice. PLoS One. 8(9):e74963. doi: 10.1371/journal.pone.0074963.
   PubMed Web of Science ®Google Scholar
• Ge XK, Wang AA, Ying ZX, Zhang LG, Su WP, Cheng K, Feng CC, Zhou YM, Zhang LL, Wang T. 2019. Effects of diets with different energy and bile acids levels on growth performance and lipid metabolism in broilers. Poult Sci. 98(2):887–895. doi: 10.3382/ps/pey434.
   PubMed Web of Science ®Google Scholar
• Kogut MH, Yin X, Yuan J, Broom L. 2017. Gut health in poultry. CAB Rev. Perspect. Agric. Vet. Sci. Nutr Nat Resour. 2017:1–7. doi: 10.1079/PAVSNNR201712031.
   Google Scholar
• Laconi A, Tolosi R, Mughini-Gras L, Cuccato M, Cannizzo FT, Piccirillo A. 2022. Amoxicillin and thiamphenicol treatments may influence the co-selection of resistance genes in the chicken gut microbiota. Sci Rep. 12(1):20413. doi: 10.1038/s41598-022-24927-7.
   PubMed Web of Science ®Google Scholar
• Li Y, Sun T, Hong Y, Qiao T, Wang Y, Li W, Tang S, Yang X, Li J, Li X, et al. 2021. Mixture of five fermented herbs (ZhihuasiTk) alters the intestinal microbiota and promotes the growth performance in piglets. Front Microbiol. 12:725196.,. doi: 10.3389/fmicb.2021.725196.
   PubMedGoogle Scholar
• Lillehoj H, Liu Y, Calsamiglia S, Fernandez-Miyakawa ME, Chi F, Cravens RL, Oh S, Gay CG. 2018. Phytochemicals as antibiotic alternatives to promote growth and enhance host health. Vet Res. 49(1):76. doi: 10.1186/s13567-018-0562-6.
   PubMedGoogle Scholar
• Liu WC, Pan ZY, Zhao Y, Guo Y, Qiu SJ, Balasubramanian B, Jha R. 2022a. Effects of heat stress on production performance, redox status, intestinal morphology and barrier-related gene expression, cecal microbiome, and metabolome in indigenous broiler chickens. Front Physiol. 13:890520. doi: 10.3389/fphys.2022.890520.
   PubMed Web of Science ®Google Scholar
• Liu ZQ, Sun X, Liu ZB, Zhang T, Zhang LL, Wu CJ. 2022b. Phytochemicals in traditional Chinese medicine can treat gout by regulating intestinal flora through inactivating NLRP3 and inhibiting XOD activity. J Pharm Pharmacol. 74(7):919–929. doi: 10.1093/jpp/rgac024.
   PubMed Web of Science ®Google Scholar
• Louis P, Scott KP, Duncan SH, Flint HJ. 2007. Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 102(5):1197–1208. doi: 10.1111/j.1365-2672.2007.03322.x.
   PubMed Web of Science ®Google Scholar
• Mund MD, Khan UH, Tahir U, Mustafa B-E, Fayyaz A. 2017. Antimicrobial drug residues in poultry products and implications on public health: a review. Int J Food Prop. 20(7):1433–1446. doi: 10.1080/10942912.2016.1212874.
   Web of Science ®Google Scholar
• Oh S, Lillehoj HS, Lee Y, Bravo D, Lillehoj EP. 2019. Dietary antibiotic growth promoters down-regulate intestinal inflammatory cytokine expression in Chickens challenged with LPS or co-infected with eimeria maxima and clostridium perfringens. Front Vet Sci. 6:420. doi: 10.3389/fvets.2019.00420.
   PubMed Web of Science ®Google Scholar
• Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, et al. 2017. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One. 12(3):e0173004. doi: 10.1371/journal.pone.0173004.
   PubMed Web of Science ®Google Scholar
• Oyenihi OR, Oyenihi AB, Erhabor JO, Matsabisa MG, Oguntibeju OO. 2021. Unravelling the anticancer mechanisms of traditional herbal medicines with metabolomics. Molecules. 26(21):6541. doi: 10.3390/molecules26216541.
   PubMed Web of Science ®Google Scholar
• Pan D, Yu Z. 2014. Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes. 5(1):108–119. doi: 10.4161/gmic.26945.
   PubMed Web of Science ®Google Scholar
• Pierre JF, Heneghan AF, Feliciano RP, Shanmuganayagam D, Roenneburg DA, Krueger CG, Reed JD, Kudsk KA. 2013. Cranberry proanthocyanidins improve the gut mucous layer morphology and function in mice receiving elemental enteral nutrition. JPEN J Parenter Enteral Nutr. 37(3):401–409. doi: 10.1177/0148607112463076.
   PubMed Web of Science ®Google Scholar
• Qian Y, Song K, Hu T, Ying T. 2018. Environmental status of livestock and poultry sectors in China under current transformation stage. Sci Total Environ. 622-623:702–709. doi: 10.1016/j.scitotenv.2017.12.045.
   PubMed Web of Science ®Google Scholar
• Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:1219.
   Web of Science ®Google Scholar
• Rizzo A, Piccinno M, Lillo E, Carbonari A, Jirillo F, Sciorsci RL. 2023. Antimicrobial resistance and current alternatives in veterinary practice: a review. Curr Pharm Des. 29(5):312–322. doi: 10.2174/1381612829666230130144731.
   PubMed Web of Science ®Google Scholar
• Roberts T, Wilson J, Guthrie A, Cookson K, Vancraeynest D, Schaeffer J, Moody R, Clark S. 2015. New issues and science in broiler chicken intestinal health: emerging technology and alternative interventions. J Appl Poult Res. 24(2):257–266. doi: 10.3382/japr/pfv023.
   Web of Science ®Google Scholar
• Rodriguez ML, Rebolé A, Velasco S, Ortiz LT, Treviño J, Alzueta C. 2012. Wheat- and barley-based diets with or without additives influence broiler chicken performance, nutrient digestibility and intestinal microflora. J Sci Food Agric. 92(1):184–190. doi: 10.1002/jsfa.4561.
   PubMed Web of Science ®Google Scholar
• Rychlik I. 2020. Composition and function of chicken gut microbiota. Animals. 10(1):103. doi: 10.3390/ani10010103.
   Web of Science ®Google Scholar
• Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 75(23):7537–7541.,. doi: 10.1128/AEM.01541-09.
   PubMed Web of Science ®Google Scholar
• Shan CH, Guo J, Sun X, Li N, Yang X, Gao Y, Qiu D, Li X, Wang Y, Feng M. 2018. Effects of fermented Chinese herbal medicines on milk performance and immune function in late-lactation cows under heat stress conditions. J Anim Sci. 96(10):4444–4457.
   PubMed Web of Science ®Google Scholar
• Shi S, Wu S, Shen Y, Zhang S, Xiao Y, He X, Gong J, Farnell Y, Tang Y, Huang Y, et al. 2018. Iron oxide nanozyme suppresses intracellular Salmonella Enteritidis growth and alleviates infection in vivo. Theranostics. 8(22):6149–6162. doi: 10.7150/thno.29303.
   PubMed Web of Science ®Google Scholar
• Slade WO, Werth EG, McConnell EW, Alvarez S, Hicks LM. 2015. Quantifying reversible oxidation of protein thiols in photosynthetic organisms. J Am Soc Mass Spectrom. 26(4):631–640. doi: 10.1007/s13361-014-1073-y.
   PubMed Web of Science ®Google Scholar
• Śliżewska K, Markowiak-Kopeć P, Żbikowski A, Szeleszczuk P. 2020. The effect of synbiotic preparations on the intestinal microbiota and her metabolism in broiler chickens. Sci Rep. 10(1):4281. doi: 10.1038/s41598-020-61256-z.
   PubMed Web of Science ®Google Scholar
• Song S, Hooiveld GJ, Zhang W, Li M, Zhao F, Zhu J, Xu X, Muller M, Li C, Zhou G. 2016. Comparative proteomics provides insights into metabolic responses in rat liver to isolated soy and meat proteins. J Proteome Res. 15(4):1135–1142. doi: 10.1021/acs.jproteome.5b00922.
   PubMed Web of Science ®Google Scholar
• Sugiharto S. 2016. Role of nutraceuticals in gut health and growth performance of poultry. J. Saudi Soc. Agric Sci. 15(2):99–111. doi: 10.1016/j.jssas.2014.06.001.
   Google Scholar
• Wang J, Zhou H. 2007. Comparison of the effects of Chinese herbs, probiotics and prebiotics with those of antibiotics in diets on the performance of meat ducks. J Anim Feed Sci. 16(1):96–103. doi: 10.22358/jafs/66730/2007.
   Web of Science ®Google Scholar
• Wang Q, Garrity GM, Tiedje JM, Cole JR. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 73(16):5261–5267. doi: 10.1128/AEM.00062-07.
   PubMed Web of Science ®Google Scholar
• Wu B, Cui H, Peng X, Fang J, Cui W, Liu X. 2012. Pathology of spleen in chickens fed on a diet deficient in methionine. Health. 04(01):32–38. doi: 10.4236/health.2012.41007.
   Google Scholar
• Xu Q, Yang Z, Chen S, Zhu W, Xiao S, Liu J, Wang H, Lan S. 2022. Effects of replacing dietary fish meal by soybean meal co-fermented using Bacillus subtilis and Enterococcus faecium on serum antioxidant indices and gut microbiota of crucian carp Carassius auratus. Fishes. 7(2):54. doi: 10.3390/fishes7020054.
   Google Scholar
• Yan Y, Du C, Li Z, Zhang M, Li J, Jia J, Li A, Qin X, Song Q. 2018. Comparing the antidiabetic effects and chemical profiles of raw and fermented Chinese Ge-Gen-Qin-Lian decoction by integrating untargeted metabolomics and targeted analysis. Chinese Med. 13:54.
   PubMed Web of Science ®Google Scholar
• Zaghari M, Sarani P, Hajati H. 2020. Comparison of two probiotic preparations on growth performance, intestinal microbiota, nutrient digestibility and cytokine gene expression in broiler chickens. J Appl Anim Res. 48(1):166–175. doi: 10.1080/09712119.2020.1754218.
   Web of Science ®Google Scholar
• Zhang T, Li Q, Cheng L, Buch H, Zhang F. 2019. Akkermansia muciniphila is a promising probiotic. Microb Biotechnol. 12(6):1109–1125. doi: 10.1111/1751-7915.13410.
   PubMed Web of Science ®Google Scholar
• Zhang T, Ji X, Lu G, Zhang F. 2021. The potential of Akkermansia muciniphila in inflammatory bowel disease. Appl Microbiol Biotechnol. 105(14-15):5785–5794. doi: 10.1007/s00253-021-11453-1.
   PubMed Web of Science ®Google Scholar
• Zhao J, Li Y, Sun M, Xin L, Wang T, Wei L, Yu C, Liu M, Ni Y, Lu R, et al. 2019. The Chinese herbal formula Shenzhu Tiaopi granule results in metabolic improvement in type 2 diabetic rats by modulating the gut microbiota. Evid Based Complement Alternat Med. 2019:6976394. doi: 10.1155/2019/6976394.
   PubMed Web of Science ®Google Scholar