Mini-Reviews in Medicinal Chemistry

Author(s): Amlan Kumar Patra*

DOI: 10.2174/1389557520666191226111405

Influence of Plant Bioactive Compounds on Intestinal Epithelial Barrier in Poultry

Page: [566 - 577] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Natural plant bioactive compounds (PBC) have recently been explored as feed additives to improve productivity, health and welfare of poultry following ban or restriction of in-feed antibiotic use. Depending upon the types of PBC, they possess antimicrobial, digestive enzyme secretion stimulation, antioxidant and many pharmacological properties, which are responsible for beneficial effects in poultry production. Moreover, they may also improve the intestinal barrier function and nutrient transport. In this review, the effects of different PBC on the barrier function, permeability of intestinal epithelia and their mechanism of actions are discussed, focusing on poultry feeding. Dietary PBC may regulate intestinal barrier function through several molecular mechanisms by interacting with different metabolic cascades and cellular transcription signals, which may then modulate expressions of genes and their proteins in the tight junction (e.g., claudins, occludin and junctional adhesion molecules), adherens junction (e.g., E-cadherin), other intercellular junctional proteins (e.g., zonula occludens and catenins), and regulatory proteins (e.g., kinases). Interactive effects of PBC on immunomodulation via expressions of several cytokines, chemokines, complement components, pattern recognition receptors and their transcription factors and cellular immune system, and alteration of mucin gene expressions and goblet cell abundances in the intestine may change barrier functions. The effects of PBC are not consistent among the studies depending upon the type and dose of PBC, physiological conditions and parts of the intestine in chickens. An effective concentration in diets and specific molecular mechanisms of PBC need to be elucidated to understand intestinal barrier functionality in a better way in poultry feeding.

Keywords: Plant bioactive compound, poultry, intestinal barrier, tight junction, permeability, intestinal immunity.

Graphical Abstract

[1]
Windisch, W.; Schedle, K.; Plitzner, C.; Kroismayr, A. Use of phytogenic products as feed additives for swine and poultry. J. Anim. Sci., 2008, 86(14), E140-E148.
[http://dx.doi.org/10.2527/jas.2007-0459] [PMID: 18073277]
[2]
Cragg, G.M.; Newman, D.J. Natural products: A continuing source of novel drug leads. Biochim. Biophys. Acta, 2013, 1830(6), 3670-3695.
[http://dx.doi.org/10.1016/j.bbagen.2013.02.008] [PMID: 23428572]
[3]
Patra, A.K. An overview of antimicrobial properties of different classes of phytochemicals.Dietary Phytochemicals and Microbes; Patra, A.K., Ed.; Springer: The Netherlands, 2012, pp. 1-32.
[http://dx.doi.org/10.1007/978-94-007-3926-0_1]
[4]
Kumar, P.; Patra, A.K. Beneficial uses of black cumin (Nigella sativa L.) seeds as a feed additive in poultry nutrition. Worlds Poult. Sci. J., 2017, 73, 872-885.
[http://dx.doi.org/10.1017/S0043933917000848]
[5]
Bento, M.H.L.; Ouwehand, A.C.; Tiihonen, K.; Lahtinen, S.; Nurminen, P.; Saarinen, M.T.; Schulze, H.; Mygind, T.; Fischer, J. Essential oils and their use in animal feeds for monogastric animals – effects on feed quality, gut microbiota, growth performance and food safety: A review. Vet. Med., 2013, 58, 449-458.
[http://dx.doi.org/10.17221/7029-VETMED]
[6]
Chowdhury, S.; Mandal, G.P.; Patra, A.K.; Samanta, I.; Kumar, P.; Samanta, A.K. Different essential oils in diets of broiler chickens: 2. Gut microbes and morphology, immune response, and some blood profile and antioxidant enzymes. Anim. Feed Sci. Technol., 2018, 236, 39-47.
[http://dx.doi.org/10.1016/j.anifeedsci.2017.12.003]
[7]
Kumar, P.; Patra, A.K.; Mandal, G.P.; Samanta, I.; Pradhan, S. Effect of black cumin seeds on growth performance, nutrient utilization, immunity, gut health and nitrogen excretion in broiler chickens. J. Sci. Food Agric., 2017, 97(11), 3742-3751.
[http://dx.doi.org/10.1002/jsfa.8237] [PMID: 28120474]
[8]
Pathak, M.; Mandal, G.P.; Patra, A.K.; Samanta, I.; Pradhan, S.; Haldar, S. Effects of dietary supplementation of cinnamaldehyde and formic acid on growth performance, intestinal microbiota and immune response in broiler chickens. Anim. Prod. Sci., 2016, 57, 821-827.
[http://dx.doi.org/10.1071/AN15816]
[9]
Turner, J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol., 2009, 9(11), 799-809.
[http://dx.doi.org/10.1038/nri2653] [PMID: 19855405]
[10]
Ulluwishewa, D.; Anderson, R.C.; McNabb, W.C.; Moughan, P.J.; Wells, J.M.; Roy, N.C. Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr., 2011, 141(5), 769-776.
[http://dx.doi.org/10.3945/jn.110.135657] [PMID: 21430248]
[11]
Scaldaferri, F.; Pizzoferrato, M.; Gerardi, V.; Lopetuso, L.; Gasbarrini, A. The gut barrier: New acquisitions and therapeutic approaches. J. Clin. Gastroenterol., 2012, 46(Suppl. 1), S12-S17.
[http://dx.doi.org/10.1097/MCG.0b013e31826ae849] [PMID: 22955350]
[12]
Patra, A.K.; Amasheh, S.; Aschenbach, J.R. Modulation of gastrointestinal barrier and nutrient transport function in farm animals by natural plant bioactive compounds - a comprehensive review. Crit. Rev. Food Sci. Nutr., 2018.
[http://dx.doi.org/10.1080/10408398.2018] [PMID: 29889546]
[13]
Alagawany, M.; Abd El-Hack, M.E.; Farag, M.R.; Shaheen, M.M.; Abdel-Latif, M.A.; Noreldin, A.E.; Patra, A.K. The usefulness of oregano and its derivatives in poultry nutrition. Worlds Poult. Sci. J., 2018, 74, 463-474.
[http://dx.doi.org/10.1017/S0043933918000454]
[14]
Van Boeckel, T.P.; Brower, C.; Gilbert, M.; Grenfell, B.T.; Levin, S.A.; Robinson, T.P.; Teillant, A.; Laxminarayan, R. Global trends in antimicrobial use in food animals. Proc. Natl. Acad. Sci. USA, 2015, 112(18), 5649-5654.
[http://dx.doi.org/10.1073/pnas.1503141112] [PMID: 25792457]
[15]
Peterson, L.W.; Artis, D. Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat. Rev. Immunol., 2014, 14(3), 141-153.
[http://dx.doi.org/10.1038/nri3608] [PMID: 24566914]
[16]
Dong, Z.L.; Wang, Y.W.; Song, D.; Hou, Y.J.; Wang, W.W.; Qi, W.T.; Yun, T.T.; Li, A.K. The effects of dietary supplementation of pre-microencapsulated Enterococcus fecalis and the extract of Camellia oleifera seed on growth performance, intestinal morphology, and intestinal mucosal immune functions in broiler chickens. Anim. Feed Sci. Technol., 2016, 212, 42-51.
[http://dx.doi.org/10.1016/j.anifeedsci.2015.11.014]
[17]
Du, E.; Wang, W.; Gan, L.; Li, Z.; Guo, S.; Guo, Y. Effects of thymol and carvacrol supplementation on intestinal integrity and immune responses of broiler chickens challenged with Clostridium perfringens. J. Anim. Sci. Biotechnol., 2016, 7, 19.
[http://dx.doi.org/10.1186/s40104-016-0079-7] [PMID: 27006768]
[18]
Ghazanfari, S.; Mohammadi, Z.; Adib Moradi, M. Effects of coriander essential oil on the performance, blood characteristics, intestinal microbiota and histological of broilers. Braz. J. Poult. Sci., 2015, 17, 419-426.
[http://dx.doi.org/10.1590/1516-635X1704419-426]
[19]
Guo, S.; Cheng, Q.; Li, Y.; Duan, R.; Hou, Y.; Yi, D.; Ding, B. Effects of dietary coated-oleum cinnamomi supplementation on the immunity and intestinal integrity of broiler chickens. Anim. Sci. J., 2018, 89(11), 1581-1590.
[http://dx.doi.org/10.1111/asj.13094] [PMID: 30175428]
[20]
Hassan, F.A.M.; Awad, A. Impact of thyme powder (Thymus vulgaris L.) supplementation on gene expression profiles of cytokines and economic efficiency of broiler diets. Environ. Sci. Pollut. Res. Int., 2017, 24(18), 15816-15826.
[http://dx.doi.org/10.1007/s11356-017-9251-7] [PMID: 28534268]
[21]
Horn, N.L.; Ruch, F.; Miller, G.; Ajuwon, K.M.; Adeola, O. Determination of the adequate dose of garlic diallyl disulfide and diallyl trisulfide for effecting changes in growth performance, total-tract nutrient and energy digestibility, ileal characteristics, and serum immune parameters in broiler chickens. Poult. Sci., 2016, 95(10), 2360-2365.
[http://dx.doi.org/10.3382/ps/pew126] [PMID: 27190110]
[22]
Sangani, K.A.; Masoudi, A.A.; Hosseini, S.A. The effects of herbal plants on Mucin2 gene expression and performance in ascetic broilers. Iran. J. Vet. Med., 2014, 8, 47-52.
[23]
Kim, D.K.; Lillehoj, H.S.; Lee, S.H.; Jang, S.I.; Lillehoj, E.P.; Bravo, D. Dietary Curcuma longa enhances resistance against Eimeria maxima and Eimeria tenella infections in chickens. Poult. Sci., 2013a, 92(10), 2635-2643.
[http://dx.doi.org/10.3382/ps.2013-03095] [PMID: 24046410]
[24]
Kim, D.K.; Lillehoj, H.S.; Lee, S.H.; Jang, S.I.; Park, M.S.; Min, W.; Lillehoj, E.P.; Bravo, D. Immune effects of dietary anethole on Eimeria acervulina infection. Poult. Sci., 2013b, 92(10), 2625-2634.
[http://dx.doi.org/10.3382/ps.2013-03092] [PMID: 24046409]
[25]
Kim, D.K.; Lillehoj, H.S.; Lee, S.H.; Lillehoj, E.P.; Bravo, D. Improved resistance to Eimeria acervulina infection in chickens due to dietary supplementation with garlic metabolites. Br. J. Nutr., 2013c, 109(1), 76-88.
[http://dx.doi.org/10.1017/S0007114512000530] [PMID: 22717023]
[26]
Lee, S.H.; Lillehoj, H.S.; Jang, S.I.; Kim, D.K.; Ionescu, C.; Bravo, D. Effect of dietary Curcuma, Capsicum and Lentinus on enhancing local immunity against Eimeria acervulina infection. J. Poult. Sci., 2010, 47, 89-95.
[http://dx.doi.org/10.2141/jpsa.009025]
[27]
Lee, S.H.; Lillehoj, H.S.; Jang, S.I.; Lillehoj, E.P.; Min, W.; Bravo, D.M. Dietary supplementation of young broiler chickens with Capsicum and turmeric oleoresins increases resistance to necrotic enteritis. Br. J. Nutr., 2013, 110(5), 840-847.
[http://dx.doi.org/10.1017/S0007114512006083] [PMID: 23566550]
[28]
Lee, Y.; Lee, S.H.; Gadde, U.D.; Oh, S.T.; Lee, S.J.; Lillehoj, H.S. Dietary Allium hookeri reduces inflammatory response and increases expression of intestinal tight junction proteins in LPS-induced young broiler chicken. Res. Vet. Sci., 2017, 112, 149-155.
[http://dx.doi.org/10.1016/j.rvsc.2017.03.019] [PMID: 28391057]
[29]
Li, H.L.; Li, Z.J.; Wei, Z.S.; Liu, T.; Zou, X.Z.; Liao, Y.; Luo, Y. Long-term effects of oral tea polyphenols and Lactobacillus brevis M8 on biochemical parameters, digestive enzymes, and cytokines expression in broilers. J. Zhejiang Univ. Sci. B, 2015, 16(12), 1019-1026.
[http://dx.doi.org/10.1631/jzus.B1500160] [PMID: 26642185]
[30]
Liu, L.; Fu, C.; Yan, M.; Xie, H.; Li, S.; Yu, Q.; He, S.; He, J. Resveratrol modulates intestinal morphology and HSP70/90, NF-κB and EGF expression in the jejunal mucosa of black-boned chickens on exposure to circular heat stress. Food Funct., 2016, 7(3), 1329-1338.
[http://dx.doi.org/10.1039/C5FO01338K] [PMID: 26843443]
[31]
Liu, S.; Song, M.; Yun, W.; Lee, J.; Lee, C.; Kwak, W.; Han, N.; Kim, H.; Cho, J. Effects of oral administration of different dosages of carvacrol essential oils on intestinal barrier function in broilers. J. Anim. Physiol. Anim. Nutr. (Berl.), 2018a, 102(5), 1257-1265.
[http://dx.doi.org/10.1111/jpn.12944] [PMID: 29968943]
[32]
Liu, H.W.; Li, K.; Zhao, J.S.; Deng, W. Effects of chestnut tannins on intestinal morphology, barrier function, pro-inflammatory cytokine expression, microflora and antioxidant capacity in heat-stressed broilers. J. Anim. Physiol. Anim. Nutr. (Berl.), 2018b, 102(3), 717-726.
[http://dx.doi.org/10.1111/jpn.12839] [PMID: 29119618]
[33]
Paraskeuas, V.V.; Mountzouris, K.C. Modulation of broiler gut microbiota and gene expression of Toll-like receptors and tight junction proteins by diet type and inclusion of phytogenics. Poult. Sci., 2019a, 98(5), 2220-2230.
[http://dx.doi.org/10.3382/ps/pey588] [PMID: 30597072]
[34]
Paraskeuas, V.; Mountzouris, K.C. Broiler gut microbiota and expressions of gut barrier genes affected by cereal type and phytogenic inclusion. Anim Nutr, 2019b, 5(1), 22-31.
[http://dx.doi.org/10.1016/j.aninu.2018.11.002] [PMID: 30899806]
[35]
Placha, I.; Simonova, M.P.; Cobanova, K.; Laukova, A.; Faix, S. Effect of Enterococcus faecium AL41 and Thymus vulgaris essential oil on small intestine integrity and antioxidative status of laying hens. Res. Vet. Sci., 2010, 89(2), 257-261.
[http://dx.doi.org/10.1016/j.rvsc.2010.03.006] [PMID: 20362314]
[36]
Placha, I.; Takacova, J.; Ryzner, M.; Cobanova, K.; Laukova, A.; Strompfova, V.; Venglovska, K.; Faix, S. Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. Br. Poult. Sci., 2014, 55(1), 105-114.
[http://dx.doi.org/10.1080/00071668.2013.873772] [PMID: 24397472]
[37]
Placha, I.; Ryzner, M.; Cobanova, K.; Faixova, Z.; Faix, S. Effects of dietary supplementation with sage (Salvia officinalis L.) essential oil on antioxidant status and duodenal wall integrity of laying strain growers. Pol. J. Vet. Sci., 2015, 18(4), 741-749.
[http://dx.doi.org/10.1515/pjvs-2015-0096] [PMID: 26812815]
[38]
Song, Z.; Cheng, K.; Zhang, L.; Wang, T. Dietary supplementation of enzymatically treated Artemisia annua could alleviate the intestinal inflammatory response in heat-stressed broilers. J. Therm. Biol., 2017, 69, 184-190.
[http://dx.doi.org/10.1016/j.jtherbio.2017.07.015] [PMID: 29037381]
[39]
Song, Z.H.; Cheng, K.; Zheng, X.C.; Ahmad, H.; Zhang, L.L.; Wang, T. Effects of dietary supplementation with enzymatically treated Artemisia annua on growth performance, intestinal morphology, digestive enzyme activities, immunity, and antioxidant capacity of heat-stressed broilers. Poult. Sci., 2018, 97(2), 430-437.
[http://dx.doi.org/10.3382/ps/pex312] [PMID: 29077887]
[40]
Ruan, D.; Wang, W.C.; Lin, C.X.; Fouad, A.M.; Chen, W.; Xia, W.G.; Wang, S.; Luo, X.; Zhang, W.H.; Yan, S.J.; Zheng, C.T.; Yang, L. Effects of curcumin on performance, antioxidation, intestinal barrier and mitochondrial function in ducks fed corn contaminated with ochratoxin A. Animal, 2019, 13(1), 42-52.
[http://dx.doi.org/10.1017/S1751731118000678] [PMID: 29644962]
[41]
Sun, Q.; Liu, D.; Guo, S.; Chen, Y.; Guo, Y. Effects of dietary essential oil and enzyme supplementation on growth performance and gut health of broilers challenged by Clostridium perfringens. Anim. Feed Sci. Technol., 2015, 207, 234-244.
[http://dx.doi.org/10.1016/j.anifeedsci.2015.06.021]
[42]
Zeinali, S.; Ghazanfari, S.; Ebrahimi, M.A. Mucin2 gene expression in the chicken intestinal goblet cells are affected by dietary essential oils. Bulg. J. Agric. Sci., 2017, 23, 134-141.
[43]
Zhang, C.; Zhao, X.H.; Yang, L.; Chen, X.Y.; Jiang, R.S.; Jin, S.H.; Geng, Z.Y. Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poult. Sci., 2017, 96(12), 4325-4332.
[http://dx.doi.org/10.3382/ps/pex266] [PMID: 29053872]
[44]
Suzuki, T. Regulation of intestinal epithelial permeability by tight junctions. Cell. Mol. Life Sci., 2013, 70(4), 631-659.
[http://dx.doi.org/10.1007/s00018-012-1070-x] [PMID: 22782113]
[45]
Plotnikov, A.; Zehorai, E.; Procaccia, S.; Seger, R. The MAPK cascades: Signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim. Biophys. Acta, 2011, 1813(9), 1619-1633.
[http://dx.doi.org/10.1016/j.bbamcr.2010.12.012] [PMID: 21167873]
[46]
Yang, X.; Liu, Y.; Yan, F.; Yang, C.; Yang, X. Effects of encapsulated organic acids and essential oils on intestinal barrier, microbial count, and bacterial metabolites in broiler chickens. Poult. Sci., 2019, 98(7), 2858-2865.
[http://dx.doi.org/10.3382/ps/pez031] [PMID: 30715522]
[47]
Liu, D.; Guo, S.; Guo, Y. Xylanase supplementation to a wheat-based diet alleviated the intestinal mucosal barrier impairment of broiler chickens challenged by Clostridium perfringens. Avian Pathol., 2012, 41(3), 291-298.
[http://dx.doi.org/10.1080/03079457.2012.684089] [PMID: 22702457]
[48]
Kaiser, M.G.; Block, S.S.; Ciraci, C.; Fang, W.; Sifri, M.; Lamont, S.J. Effects of dietary vitamin E type and level on lipopolysaccharide-induced cytokine mRNA expression in broiler chicks. Poult. Sci., 2012, 91(8), 1893-1898.
[http://dx.doi.org/10.3382/ps.2011-02116] [PMID: 22802183]
[49]
Park, E.J.; Thomson, A.B.; Clandinin, M.T. Protection of intestinal occludin tight junction protein by dietary gangliosides in lipopolysaccharide-induced acute inflammation. J. Pediatr. Gastroenterol. Nutr., 2010, 50(3), 321-328.
[http://dx.doi.org/10.1097/MPG.0b013e3181ae2ba0] [PMID: 20118807]
[50]
Amasheh, M.; Schlichter, S.; Amasheh, S.; Mankertz, J.; Zeitz, M.; Fromm, M.; Schulzke, J.D. Quercetin enhances epithelial barrier function and increases claudin-4 expression in Caco-2 cells. J. Nutr., 2008, 138(6), 1067-1073.
[http://dx.doi.org/10.1093/jn/138.6.1067] [PMID: 18492835]
[51]
Chuenkitiyanon, S.; Pengsuparp, T.; Jianmongkol, S. Protective effect of quercetin on hydrogen peroxide-induced tight junction disruption. Int. J. Toxicol., 2010, 29(4), 418-424.
[http://dx.doi.org/10.1177/1091581810366487] [PMID: 20445016]
[52]
Suzuki, T.; Tanabe, S.; Hara, H. Kaempferol enhances intestinal barrier function through the cytoskeletal association and expression of tight junction proteins in Caco-2 cells. J. Nutr., 2011, 141(1), 87-94.
[http://dx.doi.org/10.3945/jn.110.125633] [PMID: 21068182]
[53]
Shin, D.Y.; Lu, J.N.; Kim, G.Y.; Jung, J.M.; Kang, H.S.; Lee, W.S.; Choi, Y.H. Anti-invasive activities of anthocyanins through modulation of tight junctions and suppression of matrix metalloproteinase activities in HCT-116 human colon carcinoma cells. Oncol. Rep., 2011, 25(2), 567-572.
[PMID: 21165577]
[54]
Cao, M.; Wang, P.; Sun, C.; He, W.; Wang, F. Amelioration of IFN-γ and TNF-α-induced intestinal epithelial barrier dysfunction by berberine via suppression of MLCK-MLC phosphorylation signaling pathway. PLoS One, 2013, 8(5), e61944
[http://dx.doi.org/10.1371/journal.pone.0061944] [PMID: 23671580]
[55]
Higashi, N.; Kohjima, M.; Fukushima, M.; Ohta, S.; Kotoh, K.; Enjoji, M.; Kobayashi, N.; Nakamuta, M. Epigallocatechin-3-gallate, a green-tea polyphenol, suppresses Rho signaling in TWNT-4 human hepatic stellate cells. J. Lab. Clin. Med., 2005, 145(6), 316-322.
[http://dx.doi.org/10.1016/j.lab.2005.03.017] [PMID: 15976760]
[56]
Ling, K.H.; Wan, M.L.; El-Nezami, H.; Wang, M. Protective capacity of resveratrol, a natural polyphenolic compound, against deoxynivalenol-induced intestinal barrier dysfunction and bacterial translocation. Chem. Res. Toxicol., 2016, 29(5), 823-833.
[http://dx.doi.org/10.1021/acs.chemrestox.6b00001] [PMID: 27058607]
[57]
Zou, Y.; Wei, H.K.; Xiang, Q.H.; Wang, J.; Zhou, Y.F.; Peng, J. Protective effect of quercetin on pig intestinal integrity after transport stress is associated with regulation oxidative status and inflammation. J. Vet. Med. Sci., 2016a, 78(9), 1487-1494.
[http://dx.doi.org/10.1292/jvms.16-0090] [PMID: 27301842]
[58]
Zou, Y.; Xiang, Q.; Wang, J.; Peng, J.; Wei, H. Oregano essential oil improves intestinal morphology and expression of tight junction proteins associated with modulation of selected intestinal bacteria and immune status in a pig model. BioMed Res. Int., 2016b., 20165436738
[http://dx.doi.org/10.1155/2016/5436738] [PMID: 27314026]
[59]
Al-Sadi, R.; Boivin, M.; Ma, T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front. Biosci., 2009, 14, 2765-2778.
[http://dx.doi.org/10.2741/3413] [PMID: 19273235]
[60]
Lawrence, T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb. Perspect. Biol., 2009, 1(6), a001651
[http://dx.doi.org/10.1101/cshperspect.a001651] [PMID: 20457564]
[61]
Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[62]
Cao, L.; Yang, X.J.; Li, Z.J.; Sun, F.F.; Wu, X.H.; Yao, J.H. Reduced lesions in chickens with Clostridium perfringens-induced necrotic enteritis by Lactobacillus fermentum 1.20291. Poult. Sci., 2012, 91(12), 3065-3071.
[http://dx.doi.org/10.3382/ps.2012-02548] [PMID: 23155014]
[63]
Lillehoj, H.S.; Lee, K.W. Immune modulation of innate immunity as alternatives-to-antibiotics strategies to mitigate the use of drugs in poultry production. Poult. Sci., 2012, 91(6), 1286-1291.
[http://dx.doi.org/10.3382/ps.2012-02374] [PMID: 22582284]
[64]
Gessner, D.K.; Ringseis, R.; Siebers, M.; Keller, J.; Kloster, J.; Wen, G.; Eder, K. Inhibition of the pro-inflammatory NF-κB pathway by a grape seed and grape marc meal extract in intestinal epithelial cells. J. Anim. Physiol. Anim. Nutr. (Berl.), 2012, 96(6), 1074-1083.
[http://dx.doi.org/10.1111/j.1439-0396.2011.01222.x] [PMID: 21895782]
[65]
Kim, C.H.; Lee, M.A.; Kim, T.W.; Jang, J.Y.; Kim, H.J. Anti-inflammatory effect of Allium hookeri root methanol extract in LPS-induced RAW264.7 cells. J. Korean Soc. Food Sci. Nutr., 2012, 41, 1645-1648.
[http://dx.doi.org/10.3746/jkfn.2012.41.11.1645]
[66]
Kamboh, A.A.; Hang, S.Q.; Khan, M.A.; Zhu, W.Y. In vivo immunomodulatory effects of plant flavonoids in lipopolysaccharide-challenged broilers. Animal, 2016, 10(10), 1619-1625.
[http://dx.doi.org/10.1017/S1751731116000562] [PMID: 27079952]
[67]
Kim, Y.S.; Ho, S.B. Intestinal goblet cells and mucins in health and disease: Recent insights and progress. Curr. Gastroenterol. Rep., 2010, 12(5), 319-330.
[http://dx.doi.org/10.1007/s11894-010-0131-2] [PMID: 20703838]
[68]
Golder, H.M.; Geier, M.S.; Forder, R.E.; Hynd, P.I.; Hughes, R.J. Effects of necrotic enteritis challenge on intestinal micro-architecture and mucin profile. Br. Poult. Sci., 2011, 52(4), 500-506.
[http://dx.doi.org/10.1080/00071668.2011.587183] [PMID: 21919578]
[69]
Chamorro, S.; Romero, C.; Brenes, A.; Sánchez-Patán, F.; Bartolomé, B.; Viveros, A.; Arija, I. Impact of a sustained consumption of grape extract on digestion, gut microbial metabolism and intestinal barrier in broiler chickens. Food Funct., 2019, 10(3), 1444-1454.
[http://dx.doi.org/10.1039/C8FO02465K] [PMID: 30768097]
[70]
Phalipon, A.; Cardona, A.; Kraehenbuhl, J.P.; Edelman, L.; Sansonetti, P.J.; Corthésy, B. Secretory component: A new role in secretory IgA-mediated immune exclusion in vivo. Immunity, 2002, 17(1), 107-115.
[http://dx.doi.org/10.1016/S1074-7613(02)00341-2] [PMID: 12150896]
[71]
Peebles, E.D.; Jacob, R.; Branton, S.L.; Gerard, P.D. Effects of Mycoplasma gallisepticum vaccination on serum α1-acid glycoprotein concentrations in commercial layer chickens. Poult. Sci., 2014, 93(6), 1396-1402.
[http://dx.doi.org/10.3382/ps.2014-03906] [PMID: 24879689]
[72]
Placha, I.; Chrastinova, L.; Laukova, A.; Cobanova, K.; Takacova, J.; Strompfova, V.; Chrenkova, M.; Formelova, Z.; Faix, S. Effect of thyme oil on small intestine integrity and antioxidant status, phagocytic activity and gastrointestinal microbiota in rabbits. Acta Vet. Hung., 2013, 61(2), 197-208.
[http://dx.doi.org/10.1556/AVet.2013.012] [PMID: 23661388]
[73]
Kobayashi, Y.; Suzuki, M.; Satsu, H.; Arai, S.; Hara, Y.; Suzuki, K.; Miyamoto, Y.; Shimizu, M. Green tea polyphenols inhibit the sodium-dependent glucose transporter of intestinal epithelial cells by a competitive mechanism. J. Agric. Food Chem., 2000, 48(11), 5618-5623.
[http://dx.doi.org/10.1021/jf0006832] [PMID: 11087528]
[74]
Kwon, O.; Eck, P.; Chen, S.; Corpe, C.P.; Lee, J.H.; Kruhlak, M.; Levine, M. Inhibition of the intestinal glucose transporter GLUT2 by flavonoids. FASEB J., 2007, 21(2), 366-377.
[http://dx.doi.org/10.1096/fj.06-6620com] [PMID: 17172639]
[75]
Patra, A.K. Interactions of plant bioactives with nutrient transport systems in gut of livestock. Indian J. Anim. Health, 2018, 57, 125-136.
[76]
Patra, A.K.; Geiger, S.; Schraper, K.T.; Braun, H.S.; Gehlen, H.; Starke, A.; Pieper, R.; Cieslak, A.; Szumacher-Strabel, M.; Aschenbach, J.R. Effects of dietary menthol-rich bioactive lipid compounds on zootechnical traits, blood variables and gastrointestinal function in growing sheep. J. Anim. Sci. Biotechnol., 2019. (revision submitted).
[http://dx.doi.org/10.1186/s40104-019-0398-6]
[77]
Wang, H.; Liang, S.; Li, X.; Yang, X.; Long, F.; Yang, X. Effects of encapsulated essential oils and organic acids on laying performance, egg quality, intestinal morphology, barrier function, and microflora count of hens during the early laying period. Poult. Sci., 2019, 98(12), 6751-6760.
[http://dx.doi.org/10.3382/ps/pez391] [PMID: 31347675]