Isoquinolone alkaloids mitigate microscopic digestive tract lesions induced by sub-acute ruminal acidosis (SARA) in feedlot cattle
DOI:
https://doi.org/10.5433/1679-0359.2020v41n5p1567Keywords:
Chelerythrine Na , K - ATPase pump, Ruminitis, Sanguinarine.Abstract
Feedlot cattle is submitted to a diet rich in energy and reduced in fibres that induces the sub-acute ruminal acidosis (SARA) with its lesions and clinical signs. Recent studies have demonstrated some amelioration of this condition by the use of isoquinolone alkaloids found in Macleaya cordata (Papaveraceae) such as Sanguinarine and Chelerythrine. These compounds have demonstrated antimicrobial, anti-in?ammatory and immune-modulatory effects in both humans and animals The aim on this study, using histopathology and a score system, was to evaluate the differences between a non-treated and a treated group feed with these alkaloids, present in trade preparation Sangrovit-RS® as a source of sanguinarine (SG), chelerythrine (CH) and protropine (PA) standardized to 0.15% w/w SG, using feedlot cattle under a high-grain diet as an inflammatory model for gastrointestinal system. The samples of forestomachs were evaluated and graded using scores ranging from zero (0) to three (3) obtained at light-microscopic fields of 400X. Parameters such as inflammation, hydropic degeneration, hyperkeratosis, and vesicle formation were accessed in the different layers of the tissues, considering the severity and dispersion of the microscopic lesions. The soft tissues such as the abomasum, small intestine, cecum and colon had their total amount of inflammatory cells counted at light-microscopic fields of 200X. The rumen of the SG-CH-PRO-treated group showed a significant reduction in the epithelial hydropic degeneration scores (p ? 0.001) and lamina propria inflammation (p ? 0.001).The reticulum had a similar reduction in scores of epithelial (p ? 0.002) and stratum corneum hydropic degeneration (p ? 0.001), hyperkeratosis (p ? 0.002) and inflammation in lamina propria (p ? 0.001) and epithelium (p ? 0.002). The omasum had no significant differences. All non-keratinized tissues, except for ileum, had a significant decrease (p ? 0.001) in the total counting of inflammatory cells. In this trial, the feedlot cattle feed with high grain diet and treated with isoquinolone alkaloids expressed lesions that indicate ameliorations and worsening’s. Ameliorating effects of the alkaloids were better demonstrated in tissues with reduced or no corneal layer in the mucosa and in the absence of a lipopolysaccharides rich acidic environment reinforcing the notion of the topic action, the dependence of the media pH and the time of exposure modulating the pharmacological mechanisms of these alkaloids. The observed cytolytic (oncolysis) effect in epithelial forestomachs cells under low pH values, worsening the osmotic status, should be considered before clinical applications.Metrics
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References
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Estrada-Ângulo, A., Aguilar-Hernandez, A., Osuna-Perez, M., Nunez-Benitez, V. H., Castro-Perez, B. I., & Silva-Hidalgo, G. (2016). Influence of quaternary benzophenantridine and protopine alkaloids on growth performance, dietary energy, carcass traits, visceral mass, and rumen health in finishing ewes under conditions of severe temperature-humidity index. Asian-Australasian Journal of Animal Sciences, 29(5), 652-658. doi: 10.5713/ajas.15.0300.
Gonin, S., Deschenes, G., Roger, F., Bens, M., Martin, P.Y., Carpenter, JL., Feraille, E. (2001). Cyclic AMP increases cell surface expression of functional Na, K-ATPase units in mammalian cortical collecting duct principal cells. Molecular Biology of the Cell, 12(2), 255-264. doi: 10.1091/mbc.12.2.
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Herrera-Mata, H., Rosas-Romero, A., & Crescente, O. (2002). Biological activity of sanguinaria (Justicia secunda) extracts. Pharmaceutical Biology, 40(3), 206-212. doi: 10.1076/phbi.40.3.206.5826
Hu, Z.B., Xu, Y., Feng, S.C., & Guang-Jin, F. (1979). Studies on the active components from fruits of Macleaya cordata (Willd) R. Br [J]. Acta Pharmaceutica Sinica, 14(9), 535-539.
Jankowski, J., Zdunczyk, Z., Juskiewicz, J., Koztoski, K., Lecewicz, A., & Jeroch, H. (2009). Gastrointestinal tract and metabolic response of broilers to diets with the Macleaya cordata alkaloid extract. Archiv für Geflugelkunde, 73(2), 95-101.
Johnson, C. C., Jonhson, G., & Poe, C. F. (1952). Toxicity of alkaloid to certain bacteria. II. Berberine, physostigmine and sanguinarine. Acta Pharmacologica et Toxicologica, 8(1), 71-78. doi: 10.1111/j.1600-0773.1952.tb02885.x
Kosina, P., Gregorova, J., Gru, J., Vacek, J., Kolar, M., Voguel, M., & Ulrichova, J. (2010). Phytochemical and antimicrobial characterization of Macleaya cordata herb. Fitoterapia, 81(8), 1006-1012. doi: 10.1016/j.fitote.2010.06.020
Kraieski, A. L., Hayashi, R. M., Sanches, A., Almeida, G. C., & Santin, E. (2017) Effect of aflatoxin experimental ingestion and Eimeira vaccine challenges on intestinal histopathology and immune cellular dynamic of broilers: applying an Intestinal Health Index. Poultry Science, 96(5), 1078-1087. doi: 10.3382/ps/pew397
Lauf, P. K., Heinyd, J., Meller, J., Lepera, M. A., Koikovd, L., Alter, G.M., Brown, TL., & Adragna, N.C.(2013). Canonical Bcl-2 motifs of the Na+/K+ pump revealed by the BH3 mimetic chelerythrine: early signal transducers of apoptosis? Cellular Physiological Biochemistry, 31(2-3), 257-276. doi: 10.1159/000343366.
Lenfeld, J., Kroutil, M., Marsalek, E., Slavik, J., Preinningger, V., & Simanek, V. (1981). Anti-inflammatory activity of quaternary benzophenanthridine alkaloids from Chelidonium majus. Planta Medica, 43(10), 161-165. doi: 10.1055/s-2007-971493.
Mahody, G. B., Pendland, S. L., Stoia, A., & Chadwhick, L. R. (2003). In vitro susceptibility of Helicobacter pylori to isoquinoline alkaloids from Sanguinaria canadensis and Hudrastis canadensis. Phytotherapic Reserach, 17(3), 217-221. doi: 10.1002/ptr.1108.
Mendonça, F. L. M., Silva, R. J., Andrade, J. P., Ferreira, L. D., Rogge, H. I., Ferreira, L. C. A., & Facury, E. J., Fº. (2016). Assessment of dietary isoquinoline alkaloids in the prevention of cryptosporidiosis in newborn calves. Proceedings of the Congress of the World Association for Buiatrics, World Buiatrics Congress, Dublin, Irlanda, 29.
Millen, D. D., & Arrigoni, M. D. B. (2013). Drivers of change in animal protein production systems: Changes from “traditional” to “modern” beef cattle production systems in Brazil. Animal Frontiers, 3(3), 56-60. doi: 10.2527/af.2013-0025
Morgante, M., Stelletta, C., Berzaghi, P., Gianesella, M., & Andrighetto, I. (2007). Subacute rumen acidosis in lactating cows: An investigation in intensive Italian dairy herds. Journal of Animal Physiology and Animal Nutrition, 91(5-6), 226-234. doi: 10.1111/j.1439-0396.2007.00696.x
Newton, S. M., Lau, C., Gurcha, S. S., Besra, G. S., & Wright, C. W. (2002). The evaluation of forty-three plant species for in vitro anti-mycobacterial activities: isolation of active constituents from Psoralea corylifolia and Sanguinaria canadensis. Journal of Ethnopharmacology, 79(1), 57-67. doi: 10.1016/s0378-8741(01)00350-6
Oetzel, G. R. (2000). Clinical aspects of ruminal acidosis in dairy cattle. Proceedings of the RD Annual Convention of the American Association of Bovine Practitioners, Rapid City, South Dakota USA, 33.
Pitts, B. J. R., & Meyerson, L. (1981). Inhibition of Na, K‐ATPase activity and ouabain binding by sanguinarine. Drug Development Research, 1(1), 43-49. doi: 10.1002/ddr.430010105
Plaizier, J. C., Khafipour, E., Li, S., Gozho, G. N., & Krause, D. O. (2012). Subacute ruminal acidosis (SARA), endotoxins and health consequences. Animal Feed Science and Technology, 72(1-2), 9-21. doi: 10.1016/j.anifeedsci.2011.12.004
Sato, S. (2015). Subacute ruminal acidosis (SARA) challenge, ruminal condition and cellular immunity in cattle. Japanese Journal of Veterinary Research, 63(1), 25-36. doi: 10.14943/jjvr.63.suppl.s25
Slaninova, I., Taborska, E., Bochorakova, H., & Slanina, J. (2001). Interaction of benzo[c]phenanthridine and protoberberine alkaloids with animal and yeast cells. Cellular Biology Toxicolology, 17(1), 51-63. doi: 10.1023/a:1010907231602.
Straub, K. D., & Carver, P. (1975). Sanguinarine, inhibitor of NA-K dependent ATP'ASE. Biochemical and Biophysical Research Communications, 62(4), 913-922. doi: 10.1016/0006-291X(75)90410-6
Tajik, J., Nadalian, M. G., Raoofi, A., Mohammad, G. R. I., & Bahonar, A. R. (2009). Prevalence of subacute ruminal acidosis in some dairy herds of Khorasan Razavi province, northeast of Iran. Iranian Journal of Veterinary Research, 10(26), 28-32.
Vrublova, E., Vostalova, J., Ehrmann, J., Palikova, I., Vrbkova, J., Vacek, J., Simanek, V. (2010). The phytogenic feed additive Sangrovit modulates dextran sulfate sodium-induced colitis in rats. Veterinarni Medicina, 55(12), 610-618. doi: 10.17221/2945-VETMED.
Walker, C. (1990). Effect of sanguinarine and sanguinarine extract on the microbiota associated with the oral activity. Journal o. Canine. Dentistry. Association, 56(7), 13-17
Windisch, W., Schedle, K., Plitzner, C., & Kroismayr, A. (2008). Use of phytogenic products as feed additives for swine and poultry. Journal of Animal Science, 86(14), 140-148. doi: 10.2527/jas.2007-0459
Xu-Biao, L., Chen, B., & Yao, S. Z. (2006). Rapid determination of protopine, allocryptopine, sanguinarine and chelerythrine in fruits of Macleaya cordata by microwave-assisted solvent extraction and HPLC-ESI/MS [J]. Phytochemical Analysis, 17(6), 431-438. doi: 10.1002/pca.945
Zdarilova, A., Vostálová, J., Vrublova, E., & Klejdus, B. (2008). Natural feed additive of Macleaya cordata: Safety assessment in rats a 90-day feeding experiment. Food and Chemical Toxicology, 46(12), 3721-3726. doi: 10.1016/j.fct.2008.09.054
Belote, B. L., Tujimoto-Silva, A., Hummeelggen, P. H., Sanches, A. W. D., Wammes, J. C. S., Hayashi, R. M., & Santin, E. (2018). Histological parameters to evaluate intestinal health on broilers challenged with Eimeria and Clostridium perfringens with or without enramycin as growth promoter. Poultry Science, 97(7), 1-8. doi: 10.3382/ps/pey064.
Costa, V. A. C., Detmann, E., Valadares, S. C., Fº., Paulino, M. F., Henriques, L. T., & Mantovani, H. C. (2008). Degradação in vitro da fibra em detergente neutro de forragem tropical de baixa qualidade em função de suplementação com proteína e/ou carboidratos. Revista Brasileira de Zootecnia, 37(3), 494-503. doi: 10.1590/S1516-35982008000300015.
Dirksen, G. U., Liebich, H. G., & Mayer, E. (1985). Adaptive changes of the ruminal mucosa and their functional and clinical significance. The Bovine Practitioner, 20, 116-120.
Estrada-Ângulo, A., Aguilar-Hernandez, A., Osuna-Perez, M., Nunez-Benitez, V. H., Castro-Perez, B. I., & Silva-Hidalgo, G. (2016). Influence of quaternary benzophenantridine and protopine alkaloids on growth performance, dietary energy, carcass traits, visceral mass, and rumen health in finishing ewes under conditions of severe temperature-humidity index. Asian-Australasian Journal of Animal Sciences, 29(5), 652-658. doi: 10.5713/ajas.15.0300.
Gonin, S., Deschenes, G., Roger, F., Bens, M., Martin, P.Y., Carpenter, JL., Feraille, E. (2001). Cyclic AMP increases cell surface expression of functional Na, K-ATPase units in mammalian cortical collecting duct principal cells. Molecular Biology of the Cell, 12(2), 255-264. doi: 10.1091/mbc.12.2.
Hernández, J., Benedito, J. L., Abuelo, A., & Castillo, C. (2014). Ruminal acidosis in feedlot: from aetiology to prevention. The Scientific World Journal, (2014), 1-8. doi: 10.1155/2014/702572.
Herrera-Mata, H., Rosas-Romero, A., & Crescente, O. (2002). Biological activity of sanguinaria (Justicia secunda) extracts. Pharmaceutical Biology, 40(3), 206-212. doi: 10.1076/phbi.40.3.206.5826
Hu, Z.B., Xu, Y., Feng, S.C., & Guang-Jin, F. (1979). Studies on the active components from fruits of Macleaya cordata (Willd) R. Br [J]. Acta Pharmaceutica Sinica, 14(9), 535-539.
Jankowski, J., Zdunczyk, Z., Juskiewicz, J., Koztoski, K., Lecewicz, A., & Jeroch, H. (2009). Gastrointestinal tract and metabolic response of broilers to diets with the Macleaya cordata alkaloid extract. Archiv für Geflugelkunde, 73(2), 95-101.
Johnson, C. C., Jonhson, G., & Poe, C. F. (1952). Toxicity of alkaloid to certain bacteria. II. Berberine, physostigmine and sanguinarine. Acta Pharmacologica et Toxicologica, 8(1), 71-78. doi: 10.1111/j.1600-0773.1952.tb02885.x
Kosina, P., Gregorova, J., Gru, J., Vacek, J., Kolar, M., Voguel, M., & Ulrichova, J. (2010). Phytochemical and antimicrobial characterization of Macleaya cordata herb. Fitoterapia, 81(8), 1006-1012. doi: 10.1016/j.fitote.2010.06.020
Kraieski, A. L., Hayashi, R. M., Sanches, A., Almeida, G. C., & Santin, E. (2017) Effect of aflatoxin experimental ingestion and Eimeira vaccine challenges on intestinal histopathology and immune cellular dynamic of broilers: applying an Intestinal Health Index. Poultry Science, 96(5), 1078-1087. doi: 10.3382/ps/pew397
Lauf, P. K., Heinyd, J., Meller, J., Lepera, M. A., Koikovd, L., Alter, G.M., Brown, TL., & Adragna, N.C.(2013). Canonical Bcl-2 motifs of the Na+/K+ pump revealed by the BH3 mimetic chelerythrine: early signal transducers of apoptosis? Cellular Physiological Biochemistry, 31(2-3), 257-276. doi: 10.1159/000343366.
Lenfeld, J., Kroutil, M., Marsalek, E., Slavik, J., Preinningger, V., & Simanek, V. (1981). Anti-inflammatory activity of quaternary benzophenanthridine alkaloids from Chelidonium majus. Planta Medica, 43(10), 161-165. doi: 10.1055/s-2007-971493.
Mahody, G. B., Pendland, S. L., Stoia, A., & Chadwhick, L. R. (2003). In vitro susceptibility of Helicobacter pylori to isoquinoline alkaloids from Sanguinaria canadensis and Hudrastis canadensis. Phytotherapic Reserach, 17(3), 217-221. doi: 10.1002/ptr.1108.
Mendonça, F. L. M., Silva, R. J., Andrade, J. P., Ferreira, L. D., Rogge, H. I., Ferreira, L. C. A., & Facury, E. J., Fº. (2016). Assessment of dietary isoquinoline alkaloids in the prevention of cryptosporidiosis in newborn calves. Proceedings of the Congress of the World Association for Buiatrics, World Buiatrics Congress, Dublin, Irlanda, 29.
Millen, D. D., & Arrigoni, M. D. B. (2013). Drivers of change in animal protein production systems: Changes from “traditional” to “modern” beef cattle production systems in Brazil. Animal Frontiers, 3(3), 56-60. doi: 10.2527/af.2013-0025
Morgante, M., Stelletta, C., Berzaghi, P., Gianesella, M., & Andrighetto, I. (2007). Subacute rumen acidosis in lactating cows: An investigation in intensive Italian dairy herds. Journal of Animal Physiology and Animal Nutrition, 91(5-6), 226-234. doi: 10.1111/j.1439-0396.2007.00696.x
Newton, S. M., Lau, C., Gurcha, S. S., Besra, G. S., & Wright, C. W. (2002). The evaluation of forty-three plant species for in vitro anti-mycobacterial activities: isolation of active constituents from Psoralea corylifolia and Sanguinaria canadensis. Journal of Ethnopharmacology, 79(1), 57-67. doi: 10.1016/s0378-8741(01)00350-6
Oetzel, G. R. (2000). Clinical aspects of ruminal acidosis in dairy cattle. Proceedings of the RD Annual Convention of the American Association of Bovine Practitioners, Rapid City, South Dakota USA, 33.
Pitts, B. J. R., & Meyerson, L. (1981). Inhibition of Na, K‐ATPase activity and ouabain binding by sanguinarine. Drug Development Research, 1(1), 43-49. doi: 10.1002/ddr.430010105
Plaizier, J. C., Khafipour, E., Li, S., Gozho, G. N., & Krause, D. O. (2012). Subacute ruminal acidosis (SARA), endotoxins and health consequences. Animal Feed Science and Technology, 72(1-2), 9-21. doi: 10.1016/j.anifeedsci.2011.12.004
Sato, S. (2015). Subacute ruminal acidosis (SARA) challenge, ruminal condition and cellular immunity in cattle. Japanese Journal of Veterinary Research, 63(1), 25-36. doi: 10.14943/jjvr.63.suppl.s25
Slaninova, I., Taborska, E., Bochorakova, H., & Slanina, J. (2001). Interaction of benzo[c]phenanthridine and protoberberine alkaloids with animal and yeast cells. Cellular Biology Toxicolology, 17(1), 51-63. doi: 10.1023/a:1010907231602.
Straub, K. D., & Carver, P. (1975). Sanguinarine, inhibitor of NA-K dependent ATP'ASE. Biochemical and Biophysical Research Communications, 62(4), 913-922. doi: 10.1016/0006-291X(75)90410-6
Tajik, J., Nadalian, M. G., Raoofi, A., Mohammad, G. R. I., & Bahonar, A. R. (2009). Prevalence of subacute ruminal acidosis in some dairy herds of Khorasan Razavi province, northeast of Iran. Iranian Journal of Veterinary Research, 10(26), 28-32.
Vrublova, E., Vostalova, J., Ehrmann, J., Palikova, I., Vrbkova, J., Vacek, J., Simanek, V. (2010). The phytogenic feed additive Sangrovit modulates dextran sulfate sodium-induced colitis in rats. Veterinarni Medicina, 55(12), 610-618. doi: 10.17221/2945-VETMED.
Walker, C. (1990). Effect of sanguinarine and sanguinarine extract on the microbiota associated with the oral activity. Journal o. Canine. Dentistry. Association, 56(7), 13-17
Windisch, W., Schedle, K., Plitzner, C., & Kroismayr, A. (2008). Use of phytogenic products as feed additives for swine and poultry. Journal of Animal Science, 86(14), 140-148. doi: 10.2527/jas.2007-0459
Xu-Biao, L., Chen, B., & Yao, S. Z. (2006). Rapid determination of protopine, allocryptopine, sanguinarine and chelerythrine in fruits of Macleaya cordata by microwave-assisted solvent extraction and HPLC-ESI/MS [J]. Phytochemical Analysis, 17(6), 431-438. doi: 10.1002/pca.945
Zdarilova, A., Vostálová, J., Vrublova, E., & Klejdus, B. (2008). Natural feed additive of Macleaya cordata: Safety assessment in rats a 90-day feeding experiment. Food and Chemical Toxicology, 46(12), 3721-3726. doi: 10.1016/j.fct.2008.09.054
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2020-06-17
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Sanches, A. W. D., Montiani-Ferreira, F., Santin, E., Neumann, M., Reck, A. M., Bertagnon, H. G., & Pachaly, J. R. (2020). Isoquinolone alkaloids mitigate microscopic digestive tract lesions induced by sub-acute ruminal acidosis (SARA) in feedlot cattle. Semina: Ciências Agrárias, 41(5), 1567–1580. https://doi.org/10.5433/1679-0359.2020v41n5p1567
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