Effects of dietary Macleaya cordata extract on growth performance, immune responses, antioxidant capacity, and intestinal development in weaned piglets

References

• Bavarsadi M , Mahdavi AH , Ansari-Mahyari S , Jahanian E. 2016. Effects of different levels of sanguinarine on antioxidant indices, immunological responses, ileal microbial counts and jejunal morphology of laying hens fed diets with different levels of crude protein. J Anim Physiol Anim Nutr. 101:936–948. doi: 10.1111/jpn.12528
   PubMed Web of Science ®Google Scholar
• Boudry G , Péron V , HuërouLuron IL , Lallès JP , Sève B. 2004. Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J Nutr. 134:2256–2262. doi: 10.1093/jn/134.9.2256
   PubMed Web of Science ®Google Scholar
• Chaturvedi MM , Kumar A , Darnay BG , Chainy GB , Agarwal S , Aggarwal BB. 1997. Sanguinarine (pseudochelerythrine) is a potent inhibitor of NF-kappa B activation, Ikappa B alpha phosphorylation, and degradation. J Biol Chem. 272:30129–30134. doi: 10.1074/jbc.272.48.30129
   PubMed Web of Science ®Google Scholar
• Chen YP , Cheng YF , Li XH , Zhang H , Yang WL , Wen C , Zhou YM. 2016. Dietary palygorskite supplementation improves immunity, oxidative status, intestinal integrity, and barrier function of broilers at early age. Anim Feed Sci Technol. 219:200–209. doi: 10.1016/j.anifeedsci.2016.06.013
   Web of Science ®Google Scholar
• Chen JS , Kang BJ , Zhao YR , Yao K , Fu CX. 2018. Effects of natural dietary supplementation with Macleaya cordata extract containing sanguinarine on growth performance and gut health of early-weaned piglets. J Anim Physiol Anim Nutr. 102:1666–1674. doi: 10.1111/jpn.12976
   PubMed Web of Science ®Google Scholar
• Desagher S , Glowinski J , Premont J. 1996. Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci. 16:2553–2562. doi: 10.1523/JNEUROSCI.16-08-02553.1996
   PubMed Web of Science ®Google Scholar
• Drsata J , Ulrichová J , Walterová D. 1996. Sanguinarine and chelerythrine as inhibitors of aromatic amino acid decarboxylase. J Enzyme Inhib. 10:231–237. doi: 10.3109/14756369609036530
   PubMed Web of Science ®Google Scholar
• Fiesel A , Gessner DK , Most E , Eder K. 2014. Effects of dietary polyphenol-rich plant products from grape or hop on pro-inflammatory gene expression in the intestine, nutrient digestibility and faecal microbiota of weaned pigs. BMC Vet Res. 10:196. doi: 10.1186/s12917-014-0196-5
   PubMed Web of Science ®Google Scholar
• Fleury MA , Jouy E , Eono F , Cariolet R , Couet W , Gobin P , Le Goff O , Blanquet-Diot S , Alric M , Kempf I. 2016. Impact of two different colistin dosing strategies on healthy piglet fecal microbiota. Res Vet Sci. 107:152–160. doi: 10.1016/j.rvsc.2016.06.003
   PubMed Web of Science ®Google Scholar
• Frydendahl K. 2002. Prevalence of serogroups and virulence genes in Escherichia coli associated with postweaning diarrhoea and edema disease in pigs and a comparison of diagnostic approaches. Vet Microbiol. 85:169–182. doi: 10.1016/S0378-1135(01)00504-1
   PubMed Web of Science ®Google Scholar
• Gessner DK , Ringseis R , Eder K. 2017. Potential of plant polyphenols to combat oxidative stress and inflammatory processes in farm animals. J Anim Physiol Anim Nutr. 101:605–628. doi: 10.1111/jpn.12579
   PubMed Web of Science ®Google Scholar
• Goodarzi BF , Manner K , Zentek J. 2018. The impacts of Macleaya cordata extract and naringin inclusion in post-weaning piglet diets on performance, nutrient digestibility and intestinal histomorphology. Arch Anim Nutr. 72:178–189. doi: 10.1080/1745039X.2018.1459342
   PubMed Web of Science ®Google Scholar
• Gudev D , Popova RS , Moneva P. 2004. Effect of supplemental Sangrovit on some biochemical indices and leukocytes phagocytic activity in growing pigs. Arch Zootec. 7:123–134.
   Google Scholar
• Hao R , Li Q , Zhao J , Li H , Wang W , Gao J. 2015. Effects of grape seed procyanidins on growth performance, immune function and antioxidant capacity in weaned piglets. Livest Sci. 178:237–242. doi: 10.1016/j.livsci.2015.06.004
   Web of Science ®Google Scholar
• Jankowski J , ZduńCzyk Z , Juśkiewicz J , Kozłowski K , Lecewicz A , Jeroch H. 2009. Gastrointestinal tract and metabolic response of broilers to diets with the Macleaya cordata alkaloid extract. Arch Geflügelk. 73:95–101.
   Google Scholar
• Jeroch H , Kozlowski K , Jeroch J , Lipinski K , Zduńczyk Z , Jankowski J. 2009. Efficacy of the phytogenic (Papaveraceae) additive Sangrovit® in growing monogastric animals. Züchtungskunde. 81:279–293.
   Web of Science ®Google Scholar
• Johnson RJ , Kang DH , Feig D , Kivlighn S , Kanellis J , Watanabe S , Tuttle KR , Rodriguez-Iturbe B , Herrera-Acosta J , Mazzali M. 2003. Is there a pathogenetic role for uric acid in hypertension and cardiovascular and renal disease? Hypertension. 41:1183–1190. doi: 10.1161/01.HYP.0000069700.62727.C5
   PubMed Web of Science ®Google Scholar
• Juskiewicz J , Gruzauskas R , Zdunczyk Z , Semaskaite A , Jankowski J , Totilas Z , Jarule V , Sasyte V , Zdunczyk P , Raceviciute-stupeliene A , et al. 2011. Effects of dietary addition of Macleaya cordata alkaloid extract on growth performance, caecal indices and breast meat fatty acids profile in male broilers. J Anim Physiol Anim Nutr. 95:171–178. doi: 10.1111/j.1439-0396.2010.01037.x
   PubMed Web of Science ®Google Scholar
• Kantas D , Papatsiros VG , Tassis PD , Athanasiou LV , Tzika ED. 2015. Effect of a natural feed additive (Macleaya cordata), containing sanguinarine, on the performance and health status of weaning pigs. Anim Sci J. 86:92–98. doi: 10.1111/asj.12240
   PubMed Web of Science ®Google Scholar
• Kim JC , Hansen CF , Mullan BP , Pluske JR. 2012. Nutrition and pathology of weaner pigs: nutritional strategies to support barrier function in the gastrointestinal tract. Anim Feed Sci Technol. 173:3–16. doi: 10.1016/j.anifeedsci.2011.12.022
   Web of Science ®Google Scholar
• Kolpin DW , Furlong ET , Meyer MT , Thurman EM , Zaugg SD , Barber LB , Buxton HT. 2002. Pharmaceuticals, Hormones, and other organic wastewater contaminants in U.S. streams, 1999−2000: a national reconnaissance. Environ Sci Technol. 36:1202–1211. doi: 10.1021/es011055j
   PubMed Web of Science ®Google Scholar
• Kommera SK , Mateo RD , Neher FJ , Kim SW. 2006. Phytobiotics and organic acids as potential alternatives to the use of antibiotics in nursery pig diets. Asian-Aust J Anim Sci. 19:1784–1789. doi: 10.5713/ajas.2006.1784
   Web of Science ®Google Scholar
• Kong XF , Wu GY , Liao YP , Hou ZP , Liu HJ , Yin FG , Li TJ , Huang RL , Zhang YM , Deng D. 2007. Dietary supplementation with Chinese herbal ultra-fine powder enhances cellular and humoral immunity in early-weaned piglets. Livest Sci. 108:94–98. doi: 10.1016/j.livsci.2007.01.002
   Web of Science ®Google Scholar
• Kosina P , Gregorova J , Gruz J , Vacek J , Kolar M , Vogel M , Roos W , Naumann K , Simanek V , Ulrichova J. 2010. Phytochemical and antimicrobial characterization of Macleaya cordata herb. Fitoterapia. 81:1006–1012. doi: 10.1016/j.fitote.2010.06.020
   PubMed Web of Science ®Google Scholar
• Kosina P , Walterová D , Ulrichová J , Lichnovský V , Stiborová M , Rýdlová H , Vičar J , Krečman VR , Brabec MJ , Šimánek VM. 2004. Sanguinarine and chelerythrine: assessment of safety on pigs in ninety days feeding experiment. Food Chem Toxicol. 42:85–91. doi: 10.1016/j.fct.2003.08.007
   PubMed Web of Science ®Google Scholar
• Kraler M , Ghanbari M , Domig KJ , Schedle K , Kneifel W. 2016. The intestinal microbiota of piglets fed with wheat bran variants as characterised by 16S rRNA next-generation amplicon sequencing. Arch Anim Nutr. 70:173–189. doi: 10.1080/1745039X.2016.1160534
   PubMed Web of Science ®Google Scholar
• Lauridsen C. 2010. Evaluation of the effect of increasing dietary vitamin E in combination with different fat sources on performance, humoral immune responses and antioxidant status of weaned pigs. Anim Feed Sci Technol. 158:85–94. doi: 10.1016/j.anifeedsci.2010.03.015
   Web of Science ®Google Scholar
• Lee KW , Kim JS , Oh ST. 2015. Effects of dietary sanguinarine on growth performance, relative organ weight, cecal microflora, serum cholesterol level and meat quality in broiler chickens. J Poult Sci. 52:15–22. doi: 10.2141/jpsa.0140073
   Web of Science ®Google Scholar
• Lenfeld J , Kroutil M , Marsálek E , Slavík J , Preininger V , Simánek V. 1981. Antiinflammatory activity of quaternary benzophenanthridine alkaloids from Chelidonium majus. Planta Med. 43:161–165. doi: 10.1055/s-2007-971493
   PubMed Web of Science ®Google Scholar
• Li LL , Wu X , Peng HZ , Fan MZ , Hou ZP , Kong XF , Yin YL , Zhang B , Li TJ , Hou YQ , et al. 2009. The effect of dietary addition of a polysaccharide from Atractylodes macrophala Koidz on growth performance, immunoglobulin concentration and IL-1β expression in weaned piglets. J Agr Sci. 147:625–631. doi: 10.1017/S002185960999013X
   Web of Science ®Google Scholar
• Li LL , Yin FG , Zhang B , Peng HZ , Li FN , Zhu NS , Hou DX , Yin YL , Luo JJ , Tang ZR. 2011. Dietary supplementation with Atractylodes Macrophala Koidz polysaccharides ameliorate metabolic status and improve immune function in early-weaned pigs. Livest Sci. 142:33–41. doi: 10.1016/j.livsci.2011.06.013
   Web of Science ®Google Scholar
• Liu G , Guan G , Fang J , Martinez Y , Chen S , Bin P , Duraipandiyan V , Gong T , Tossou MC , Al-Dhabi NA , et al. 2016. Macleaya cordata extract decreased diarrhea score and enhanced intestinal barrier function in growing piglets. Biomed Res Int. 2016:1069585.
   PubMed Web of Science ®Google Scholar
• Liu Y , Jiao R , Ma ZG , Liu W , Wu QQ , Yang Z , Li FF , Yuan Y , Bian ZY , Tang QZ. 2015. Sanguinarine inhibits angiotensin II-induced apoptosis in H9c2 cardiac cells via restoring reactive oxygen species-mediated decreases in the mitochondrial membrane potential. Mol Med Rep. 12:3400–3408. doi: 10.3892/mmr.2015.3841
   PubMed Web of Science ®Google Scholar
• Mellor S. 2001. Natural appetisers from plants. Feed Mix. 9:29–31.
   Google Scholar
• Metzler-Zebeli BU , Schmitz-Esser S , Mann E , Grüll D , Molnar T , Zebeli Q. 2015. Adaptation of the cecal bacterial microbiome of growing pigs in response to resistant starch type 4. Appl Environ Microbiol. 81:8489–8499. doi: 10.1128/AEM.02756-15
   PubMed Web of Science ®Google Scholar
• Miao F , Yang XJ , Zhou L , Hu HJ , Zheng F , Ding XD , Sun DM , Zhou CD , Sun W. 2011. Structural modification of sanguinarine and chelerythrine and their antibacterial activity. Nat Prod Res. 25:863–875. doi: 10.1080/14786419.2010.482055
   PubMed Web of Science ®Google Scholar
• Nagy B , Arp LH , Moon HW , Casey TA. 1992. Colonization of the small intestine of weaned pigs by enterotoxigenic Escherichia coli that lack known colonization factors. Vet Pathol. 29:239–246. doi: 10.1177/030098589202900308
   PubMed Web of Science ®Google Scholar
• Newton SM , Lau C , Gurcha SS , Besra GS , Wright CW. 2002. The evaluation of forty-three plant species for in vitro antimycobacterial activities; isolation of active constituents from Psoralea corylifolia and Sanguinaria Canadensis . J Ethnopharmacol. 79:57–67. doi: 10.1016/S0378-8741(01)00350-6
   PubMed Web of Science ®Google Scholar
• Ni H , Martínez Y , Guan G , Rodríguez R , Más D , Peng H , Navarro MV , Gang L. 2016. Analysis of the impact of isoquinoline alkaloids, derived from Macleaya cordata extract, on the development and innate immune response in swine and poultry. Biomed Res Int. 2016:1352146. doi: 10.1155/2016/1352146
   PubMed Web of Science ®Google Scholar
• Niedernhofer LJ , Daniels JS , Rouzer CA , Greene RE , Marnett LJ. 2003. Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells. J Biol Chem. 278:31426–31433. doi: 10.1074/jbc.M212549200
   PubMed Web of Science ®Google Scholar
• Niu X , Fan T , Li W , Wei X , Huang H. 2012. The anti-inflammatory effects of sanguinarine and its modulation of inflammatory mediators from peritoneal macrophages. Eur J Pharmacol. 689:262–269. doi: 10.1016/j.ejphar.2012.05.039
   PubMed Web of Science ®Google Scholar
• NRC . 2012. Nutrient requirements of swine, 11th rev. ed. Washigton (DC ): Natl. Acad. Press.
   Google Scholar
• Pellikaan WF , Andrés-Elias N , Durand A , Bongers LJGM , SvL-v S , Torrallardona D. 2010. Effect of carob bean gum, spray dried porcine plasma and sanguinarine on fermentation activity in the gut of weanling pigs. Livest Sci. 133:164–168. doi: 10.1016/j.livsci.2010.06.054
   Web of Science ®Google Scholar
• Pickler L , Beirão BCB , Hayashi RM , Durau JF , Lourenço MC , Caron LF , Santin E. 2013. Effect of sanguinarine in drinking water on Salmonella control and the expression of immune cells in peripheral blood and intestinal mucosa of broilers. J Appl Poultry Res. 22:430–438. doi: 10.3382/japr.2012-00649
   Web of Science ®Google Scholar
• Pieper R , Janczyk P , Zeyner A , Smidt H , Guiard V , Souffrant WB. 2008. Ecophysiology of the developing total bacterial and lactobacillus communities in the terminal small intestine of weaning piglets. Microb Ecol. 56:474–483. doi: 10.1007/s00248-008-9366-y
   PubMed Web of Science ®Google Scholar
• Pluske JR. 2013. Feed-and feed additives-related aspects of gut health and development in weanling pigs. J Anim Sci Biotechnol. 4:83–89. doi: 10.1186/2049-1891-4-1
   Web of Science ®Google Scholar
• Pluske JR , Hampson DJ , Williams IH. 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest Prod Sci. 51:215–236. doi: 10.1016/S0301-6226(97)00057-2
   Google Scholar
• Psotova J , Vecera R , Zdarilova A , Anzenbacherova E , Kosina P , Svobodova A , Hrbac J , Jirovsky D , Stiborova M , Lichnovsky V. 2006. Safety assessment of sanguiritrin, alkaloid fraction of Macleaya cordata, in rats. Vet Med. 51:145–155. doi: 10.17221/5534-VETMED
   Web of Science ®Google Scholar
• Qi H , Xiang Z , Han G , Yu B , Huang Z , Chen D. 2011. Effects of different dietary protein sources on cecal microflora in rats. Afr J Biotechnol. 10:3704–3708.
   Google Scholar
• Qin F , Patel R , Yan C , Liu W. 2006. NADPH oxidase is involved in angiotensin II-induced apoptosis in H9C2 cardiac muscle cells: effects of apocynin. Free. Radical Bio Med. 40:236–246. doi: 10.1016/j.freeradbiomed.2005.08.010
   PubMed Web of Science ®Google Scholar
• Schwarz S , Kehrenberg C , Walsh TR. 2001. Use of antimicrobial agents in veterinary medicine and food animal production. Int J Antimicrob Agents. 17:431–437. doi: 10.1016/S0924-8579(01)00297-7
   PubMed Web of Science ®Google Scholar
• Shi YH , Wang J , Guo R , Wang CZ , Yan XB , Xu B , Zhang DQ. 2014. Effects of alfalfa saponin extract on growth performance and some antioxidant indices of weaned piglets. Livest Sci. 167:257–262. doi: 10.1016/j.livsci.2014.05.032
   Web of Science ®Google Scholar
• Spreeuwenberg MA , Verdonk JM , Gaskins HR , Verstegen MW. 2001. Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. J Nutr. 131:1520–1527. doi: 10.1093/jn/131.5.1520
   PubMed Web of Science ®Google Scholar
• Sun P , Li D , Li Z , Dong B , Wang F. 2008. Effects of glycinin on IgE-mediated increase of mast cell numbers and histamine release in the small intestine. J Nutr Biochem. 19:627–633. doi: 10.1016/j.jnutbio.2007.08.007
   PubMed Web of Science ®Google Scholar
• Tanaka T , Metori K , Mineo S , Hirotani M , Furuya T , Kobayashi S. 1993. Inhibitory effects of berberine-type alkaloids on elastase. Planta Med. 59:200–202. doi: 10.1055/s-2006-959651
   PubMed Web of Science ®Google Scholar
• Tao X , Xu ZR , Wang YZ. 2014. Effects of dietary fluoride levels on growth, serum indexes and antioxidant systems in growing pigs. Turk J Vet Anim Sci. 30:65–70.
   Google Scholar
• Vieira SL , Berres J , Reis RN , Oyarzabal OA , Coneglian JLB , Freitas DM , Peña JEM , Torres CA. 2008. Studies with sanguinarine like alkaloids as feed additive in broiler diets. Brazi J Poult Sci. 10:67–71. doi: 10.1590/S1516-635X2008000100010
   Web of Science ®Google Scholar
• 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. doi: 10.3382/ps.2008-00533
   PubMed Web of Science ®Google Scholar
• Wang M , Yang J , Gai Z , Huo S , Zhu J , Li J , Wang R , Xing S , Shi G , Shi F. 2017. Comparison between digital PCR and real-time PCR in detection of Salmonella typhimurium in milk. Int J Food Microbiol. 266:251–256. doi: 10.1016/j.ijfoodmicro.2017.12.011
   PubMed Web of Science ®Google Scholar
• Wang DF , Zhou LL , Zhou HL , Hou GY , Zhou X , Li W. 2016. Effects of Piper sarmentosum extract on the growth performance, antioxidant capability and immune response in weaned piglets. J Anim Physiol Anim Nutr. 101:105–112. doi: 10.1111/jpn.12517
   PubMed Web of Science ®Google Scholar
• Wittig W , Klie H , Gallien P , Lehmann S , Timm M , Tschäpe H. 1995. Prevalence of the fimbrial antigens F18 and K88 and of enterotoxins and verotoxins among Escherichia coli isolated from weaned pigs. Zentralbl Bakteriol. 283:95–104. doi: 10.1016/S0934-8840(11)80895-9
   PubMedGoogle Scholar
• Xu Y , Wang Z , Wang Y , Yan S , Shi B. 2018. Effects of chitosan as growth promoter on diarrhea, nutrient apparent digestibility, fecal microbiota and immune response in weaned piglets. J Appl Anim Res. 46:1437–1442. doi: 10.1080/09712119.2018.1531763
   Web of Science ®Google Scholar
• Xue GD , Wu SB , Choct M , Pastor A , Steiner T , Swick RA. 2017. Impact of a Macleaya cordata-derived alkaloid extract on necrotic enteritis in broilers. Poult Sci. 96:3581–3585. doi: 10.3382/ps/pex164
   PubMed Web of Science ®Google Scholar
• Yakhkeshi S , Rahimi S , Naseri KG. 2011. The effects of comparison of herbal extracts, antibiotic, probiotic and organic acid on serum lipids, immune response, GIT microbial population, intestinal morphology and performance of broilers. J Med Plants Res. 10:80–95.
   Google Scholar
• Yao K , Guan S , Li TJ , Huang RL , Wu GY , Ruan Z , Yin YL. 2011. Dietary L-arginine supplementation enhances intestinal development and expression of vascular endothelial growth factor in weanling piglets. Brit J Nutr. 105:703–709. doi: 10.1017/S000711451000365X
   PubMed Web of Science ®Google Scholar
• Yin J , Wu MM , Xiao H , Ren WK , Duan JL , Yang G , Li TJ , Yin YL. 2014. Development of an antioxidant system after early weaning in piglets. J Anim Sci. 92:612–619. doi: 10.2527/jas.2013-6986
   PubMed Web of Science ®Google Scholar
• Yiu CK , Wei SH. 1993. Clinical efficacy of dentifrices in the control of calculus, plaque, and gingivitis. Quintessence Int. 24:181–188.
   PubMedGoogle Scholar
• Zdarilova A , Vrublova E , Vostalova J , Klejdus B , Stejskal D , Proskova J , Kosina P , Vecera R , Hrbac J , Cernochova D , et al. 2008. Natural feed additive of Macleaya cordata: safety assessment in rats a 90-day feeding experiment. Food Chem Toxicol. 46:3721–3726. doi: 10.1016/j.fct.2008.09.054
   PubMed Web of Science ®Google Scholar
• Zhang SM , Coultas KA. 2013. Identification of plumbagin and sanguinarine as effective chemotherapeutic agents for treatment of schistosomiasis. Int J Parasitol Drugs Drug Resist. 3:28–34. doi: 10.1016/j.ijpddr.2012.12.001
   PubMed Web of Science ®Google Scholar
• Zhang C , Ling F , Chi C , Wang GX. 2013. Effects of praziquantel and sanguinarine on expression of immune genes and susceptibility to Aeromonas hydrophila in goldfish (Carassius auratus) infected with Dactylogyrus intermedius. Fish Shellfish Immunol. 35:1301–1308. doi: 10.1016/j.fsi.2013.08.001
   PubMed Web of Science ®Google Scholar
• Zhao P , Zhang Z , Lan R , Li T , Kim IH. 2018. Comparison of efficacy of lactic acid bacteria complex and Enterococcus faecium DSM 7134 in weanling pigs. J Appl Anim Res. 46:888–892. doi: 10.1080/09712119.2017.1420655
   Web of Science ®Google Scholar
• Zhu LH , Zhao KL , Chen XL , Xu JX. 2012. Impact of weaning and an antioxidant blend on intestinal barrier function and antioxidant status in pigs. J Anim Sci. 90:2581–2589. doi: 10.2527/jas.2011-4444
   PubMed Web of Science ®Google Scholar