Presencia de hongos y contaminación con micotoxinas en ensilajes para alimentación de rumiantes. Artículo de Revisión

  • Carlos Alpízar Solís Universidad Nacional Escuela de Medicina Veterinaria Departamento de Nutrición Animal
Palabras clave: hongos, ensilajes, micotoxinas, ganado, forrajes, contaminación por hongos

Resumen

Diversos estudios han identificado el crecimiento de hongos en forrajes ensilados para alimentar rumiantes domésticos, capaces de producir toxinas de importancia para la salud pública y animal.El objetivo de esta revisión es recopilar los resultados de diversas investigaciones que identificaron hongos y micotoxinas con riesgo conocido en ensilajes de diversos materiales en varias regiones del mundo utilizados para alimentar rumiantes. En segundo lugar, describir las especies de hongos más comúnmente identificadas por diversos autores en alimentos ensilados para rumiantes, y los factores que favorecen su presencia y desarrollo, con la consecuente producción de micotoxinas. Por último, describir algunas medidas para prevenir la contaminación de los ensilajes con micotoxinas, y se muestra la necesidad de realizar investigaciones relacionadas con la presencia de micotoxinas en alimentos para rumiantes en Costa Rica.Los principales efectos en rumiantes de las micotoxinas encontradas en los ensilajes se asocian a alteraciones reproductivas y del sistema inmunológico, así como del sistema digestivo. Los principales géneros identificados en los estudios revisados alrededor del mundo son Penicillium spp, Fusarium spp y Aspergillus spp. Diversos estudios reportan la contaminación de ensilajes principalmente con aflatoxinas (AFB1), fumonisinas (FB1), tricotecenos (DON, T2) y zearalenona. Factores como la presencia de oxígeno durante el ensilaje, la temperatura ambiental, el embalado y el manejo postcosecha de los forrajes tienen una importancia notable como facilitadores del desarrollo de los hongos y la consecuente producción de toxinas.

Descargas

La descarga de datos todavía no está disponible.

Citas

Alonso V., Pereyra, C., Keller, L., Dalcero, A., Rosa, C., Chiacchiera S. & Cavaglieri, L. 2013. Fungi and mycotoxins in silage: an overview. J Appl Microbiol. 115 (3): 367-643. doi: 10.1111/jam.12178.

Araya, O. 2011. Problemas tóxicos de bovinos asociados con forrajes conservados y piensos [en línea]: http://www2.inia.cl/medios/biblioteca/seriesinia/NR23515.pdf. (Consulta 10 mar. 2015).

Auerbach, H. 2003. Mould growth and mycotoxin contamination of silages: sources, types and solutions. In: Lyons T., Jacques K. (ed) Proceedings of Alltech’s Nineteenth Annual Symposium. p: 247-265.

Baliukoniene, V., Bakutis, B., Vaivadaite, T., Bartkienė, E. & Jovaišienė, J. 2012. Prevalence of fungi and mycotoxins in silage and milk in Lithuania. Vet Med Zoot. 59 (81): 9 p.

Bandera, E., Chandran, U., Buckley, B., Lin, Y., Isukapalli, S., Marshall, I., King, M. & Zarbl, H. 2011. Urinary Mycoestrogens, Body Size and Breast Development in New Jersey Girls. Sci Total Environ. 409 (24): 5221-5227. doi: 10.1016/j.scitotenv.2011.09.029.

Battacone G., Nudda, A. & Pulina, G. 2010. Effects of Ochratoxin A on Livestock Production. Toxins. 2 (7): 1796-1824. doi: 10.3390/toxins2071796.

Berthiller, F., Crews, C., Dall’asta, C., De Saeger, S., Haesaert, G., Karlovsky, P., Oswald, I., Seefelder, W., Speijers, G. & Stroka, J. 2013. Masked mycotoxins: a review. Mol. Nutr. Food Res. 57 (1):165-186. doi: 10.1002/mnfr.201100764.

Blank, R. & Wolffram, S. 2009. Effects of live yeast cell supplementation to high concentrate diets on the toxicokinetics of ochratoxin A in sheep. Food Add & Cont. 26 (1): 119–26. doi: 10.1080/02652030802320600.

Bloomquist, C., Davidson, J. & Pearson, E. 1982. Zearalenone toxicosis in prepubertal dairy heifers. J Am Vet Med Assoc. 189: 164-165.

Cámara Nacional de Productores de Leche. 2013. Proyecto: “Red Nacional de Pastos y Forrajes” [en línea]: http://www.proleche.com/recursos/documentos/RED_NACIONAL_DE_PASTOS_Y_FORRAJES.pdf (Consulta: 6 mar. 2015).

Cook, W., Richard, J., Osweiler, G. & Trampel, D. 1986. Clinical and pahtologic changes in acute bovine aflatoxicosis: rumen motility and tissue and fluid concentrations of aflatoxins B1 and M1. Am J Vet Res 47: 1187-1825.

Comité Regional de Recursos Hidráulicos (CRRH), Sistema de la Integración Centroamericana (SICA). 2014. XLIV Foro del Clima de América Central [en línea]:http://www.proleche.com/recursos/documentos/medioAmbiente/PerspectivadelClima.pdf (Consulta: 6 mar. 2015).

Coppock, R., Mostrom, M., Sparling, C., Jacobsen, B. & Ross, C. 1990. Apparent zearalenone intoxication in a dairy herd from feeding spoiled acid-treated corn. Vet Hum Toxicol. 32 (3): 246-248.

Coppock, R., Christian, R. & Jacobsen, B. 2012. Aflatoxins. P 1186-1188. In: R. Gupta (ed). Veterinary Toxicology. Ed.. 2ª edición. Elsiever. Oxford, Estados Unidos.

De Mil, T., Devreese, M., De Baere, S., Van Ranst, E., Eeckhout, M., De Backer, P. & Crobels, S. 2015. Characterization of 27 Mycotoxin Binders and the Relation with in Vitro Zearalenone Adsorption at a Single Concentration. Toxins. 7: 21-33. doi: 10.3390/toxins7010021.

Dogi, C., Armando, R., Ludueña, R., De Moreno, A., Rosa, C., Dalcero, A., & Cavaglieri, L. 2011. Saccharomyces cerevisiae strains retain their viability and aflatoxin B1 binding ability under gastrointestinal conditions and improve ruminal fermentation. Food Add & Cont. 28 (12): 1705–11. doi: 10.1080/19440049.2011.605771.

Driehuis, F. & Oude S. 2000. The impact of the quality of silage on animal health and food safety: a review. Vet Q. 22 (4): 212-216.

Duarte, S. & Villamil, L. 2006. Micotoxinas en la Salud Pública. Rev. Salud Pública. 8 (1): 129-135.

Eckard, S., Wettstein, F., Forrer, H. & Vogelgsang, S. 2011. Incidence of Fusarium species and mycotoxins in maize silage. Toxins. 3 (8): 949–67. doi: 10.3390/toxins3080949.

Engels, R. & Krämer, J. 1996. Incidence of Fusaria and occurrence of selected Fusarium mycotoxins on Lolium spp. in Germany. Mycotoxin Res. 12 (1): 31-40. doi: 10.1007/BF03192078.

Fenlon, D. & Wilson, J. 1998. The quantitative assessment of Listeria monocytogenes growth in a laboratory ensiling system allowing limited aerobic spoilage. Grass and Forage Science. 53: 292-295. doi: 10.1046/j.1365-2494.1998.00132.x.

Fink-Gremmels, J. 2005. Mycotoxins in forages. In: Diaz D.E. (ed) The mycotoxin blue book. Nottingham University Press, Nottingham, United Kingdom. p: 249-268.

Fink-Gremmels, J. & Malekinejad, H. 2007. Clinical effects and biochemical mechanisms associated with exposure to the mycoestrogen zearalenone. Anim Feed Sci Technol. 137 (3/4): 326-341. doi: 10.1016/j.anifeedsci.2007.06.008.

Forsell, J. & Petska, J. 1985. Relation of 8-ketotrichothecene and Zearalenone analog structure to inhibition of mitogen-induced human lymphocyte blastogenesis. Appl Environ Microbiol. 50: 1304-1307.

Frobish, R., Bradley, B., Wagner, D., Long-Bradley, P. & Hairston H. 1986. Aflatoxin residues in milk of dairy cattle after ingestion of naturally contaminted grain. J Food Pro. 49: 781-785.

González, M., Alonso, V., Sager, R., Morlaco, M., Magnoli, C., Astoreca, A., Rosa, C., Chiacchiera, S., Dalcero, A., & Cavaglieri, L. 2008. Fungi and selected mycotoxins from pre- and postfermented corn silage. J. Appl. Microbiol. 104 (4): 1034–41.

Gotlieb, A. 2004. Mycotoxins in silage: A silent loss in profits [en línea]: http://www.uvm.edu/pss/vtcrops/articles/Mycotoxins.html (Consulta 9 mar. 2015).

Hassan, M., Fatemeh, R. & Kobra, B. 2010. Zearalenone is bioactivated in the river Buffalo (Bubalus bubalis): hepatic biotransformation. Trop Anim Health Prod. 42 (6): 1229-1234. doi: 10.1007/s11250-010-9554-x.

Höhler, D., Südekum, K., Wolffram, S., Frohlich, A. & Marquardt, R.. 1999. Metabolism and excretion of ochratoxin A fed to sheep. J Anim Sci. 77: 1217-1223. doi: /1999.7751217x.

Huff, W., Harvey, B., Kubena, L., Rottinghaus, G. 1988. Toxic synergism between aflatoxin and T-2 toxin in broiler chickens. Poult Sci. 67 (10): 1418-1423. doi: 10.3382/ps.0671418.

Hult, K., Teiling, A., Gatenbeck, S. 1976. Degradation of ochratoxin A by a ruminant. Appl Environ Microbiol. 32: 443-444.

Johansson, M., Emmoth, E., Salomonsson, A. & Albihn, A. 2005. Potential risks when spreading anaerobic digestion residues on grass silage crops–survival of bacteria, moulds and viruses. Grass and Forage Science. 60: 175-185. doi: 10.1111/j.1365-2494.2005.00466.x.

Jouany, J. & Diaz, D. 2005. Effects of mycotoxins in ruminants. The Mycotoxin Blue Book. Diaz D., Ed. Nottingham University Press. Nottingam, Inglaterra. Pp: 295-321.

Katzenellenbogen, B., Katzenellenbogen, J. & Mordecai, D. 1979. Zearalenones: characterization of the estrogenic potencies and receptor interactions of a series of a fungar resorcyclic acid lactones. Endocrinology. 105: 33-40.

Keller, M., Keller, K., Monge, M., Pereyra, C., Alonso, V., Cavaglieri, L., Chiachiera, S. & Rosa, C. 2012. Gliotoxin contamination in pre- and postfermented corn, sorgum and wet brewer’s grains silage in Sao Paulo and Rio de Janeiro State, Brazil. J. Appl. Microbiol. 112 (5): 865-873. doi: 10.1111/j.1365-2672.2012.05273.x.

Keller, T., Nonn, H. & Jeroch, H. 1998. The Effect of Sealing and of additives on the fermentation characteristics and mould and yeast counts in stretch film wrapped big-bale lucerne silage. Arch. Anim. Nutr. 51: 63-75.

Kiessling, K., Patterson, H., Sandholm, K. & Olsen, M. 1984. Metabolism of aflatoxin, ochratoxin, zearalenonaralenone, and three trichothecenes by intact rumen fluid, rumen protozoa, and bacteria. Appl Envirn Microbiol. 47: 1070-1073.

Korosteleva, S., Smith, T. & Boermans, H. 2007. Effects of feedborne Fusarium mycotoxins on the performance, metabolism, and inmunity of dairy cows. J. Dairy Sci. 90 (8): 3867-3873.

Kuilman, M., Maas, M., Judah, J. & Fink-Gremels, J. 1998. Bovine hepatic metabolism of aflatoxin B1. J Agric Food Che. 46: 2707-2713. doi: 10.1021/jf980062x.

Kung, L. 2001. Silage fermentation and additives. In: Lyons T., Jacques K. (ed) Proceedings of Alltech’s Seventeenth Annual Symposium. p.145-159.

Madhyastha, M., Marquardt, R. & Abramson, D. 1994. Structure-activity relationships and interactions among trichothecene mycotoxins as assessed by yeast bioassay. Toxicon. 32 (9):1147-1152. doi: 10.1016/0041-0101(94)90398-0.

Manafi, M., Umakantha, B., Mohan, K. & Narayana, H. 2012. Synergistic effects of two commonly contaminating mycotoxins (aflatoxin and T-2 toxin) on biochemical parameters and inmune status of broiler chickens. World App Sci J. 17 (3): 364-367.

Mansfield, M., Archibald, D., & Jones, A. 2007. Relationship of Sphinganine Analog Mycotoxin Contamination in Maize Silage to Seasonal Weather Conditions and to Agronomic and Ensiling Practices. Phytopatology. 97 (4): 504-511. doi: http://dx.doi.org/10.1094/PHYTO-97-4-0504.

Mansfield, M. & Kuldau, G. 2007. Microbiological and molecular determination of mycobiota in fresh and ensiled maize silage. Mycologia. 99 (2): 269-278.

Miller, D. 2008. Mycotoxins in small grains and maize: old problems, new challenges. Food Add. Cont. 25 (2): 219–30. doi: 10.1080/02652030701744520.

Mostrom, M. 2012. Zearalenone. P 1267-1268. In: R. Gupta (ed). Veterinary Toxicology. Ed. 2ª edición. Elsiever. Oxford, Estados Unidos.

Mostrom, M. & Raisbeck, M. 2012. Tricothecenes. p 1242-1257. In: R. Gupta (ed). Veterinary Toxicology. Ed.. 2ª edición. Elsiever. Oxford, Estados Unidos.

Müller, H. & Amend, R. 1997. Formation and disappearance of mycophenolic acid, patulin, penicillic acid and PR toxin in maize silage inoculated with Penicillium roqueforti. Arch. Anim. Nutr. 50 (1): 213-225. doi: 10.1080/17450399709386133.

Nešic, S., Grubic, G., Adamovic, M., Ðorðevic, N., Stojanovic, B. & Bo, A. 2010. Uso de la zeolita como absorbente de la zearalenona en la nutrición de terneros. Rev. Cub. Cienc. Agrícol. 44 (3): 227–233.

Nielson, A. 2012. Aflatoxin testing not a foolproof solution. South east farm press.7 noviembre.

Notermans, S., Kozaki, S. & Van Schothorst, M. 1979. Toxin production by Clostridium botulinum in grass. Appl Environ Microbiol. 38 (5): 767-771.

O’ Brien, M., Kiely, P., Forristal, P. & Fuller, H. 2008. Fungal contamination of big-bale grass silage on irish farms : predominant mould and yeast species and features of bales and silage. Grass and Forage Science. 63: 121–137.

Osuna, O., Edds, G. & Blankespoor, H. 1977. Toxic effects of aflatoxin B1 in male Holstein calves with prior infection by flukes (Fasciola hepatica). Am J Vet Res. 38: 341-349.

Ovando, M., Ozsisli, B., Anderson, J., Whitney, K., Ohm, J. & Simsek, S. 2013. Analysis of deoxynivalenol and deoxynivalenol-3-glucoside in hard red spring wheat inoculated with Fusarium graminearum. Toxins. 5 (12): 2522-2532. doi: 10.3390/toxins5122522.

Osweiler, G., Kehrli, M., Stabel, J., Thurston, J., Ross, F. & Wilson, T. 1993. Effects of fumonisin-contaminated corn screenings on growth and health of feeder calves. J Anim Sci. 71 (1): 459-466.

Peña, G., Pereyra, C., Armando, M., Chiacchiera, S., Magnoli, C., Orlando, J., Dalcero, A., Rosa, C. & Cavaglieri, L. 2010. Aspergillus fumigatus toxicity and gliotoxin levels in feedstuff for domestic animals and pets in Argentina. Letters in Applied Microbiology. 50 (1): 77–81. doi: 10.1111/j.1472-765X.2009.02756.x.

Poapolathep, A., Kumagai, S., Suzuki, H. & Doi, K. 2004 (a). Development of early apoptosis and changes in T-cell subsets in mouse thymocyte primary cultures treated with nivalenol. Exp Mol Pathol. 77 (2): 149-152. doi: 10.1016/j.yexmp.2004.04.004.

Poapolathep, A., Nagata, T., Suzuki, H., Kumagai, S. & Doi, K. 2003. Development of early apoptosis and changes in lymphocyte subsets in lymphoid organs in mice orally inoculated with nivalenol. Exp. Mol. Pathol. 75 (1): 74-79. doi: 10.1016/S0014-4800(03)00027-3.

Poapolathep, A., Sugita-konishi, Y., Phitsanu, T., Doi, K. & Kumagai, S.. 2004 (b). Placental and milk transmission of trichothecene mycotoxins, nivalenol and fusarenon X, in mice. Toxicon. 44 (1): 111-113. doi: 10.1016/j.toxicon.2004.04.005.

Puel, O., Tadrist, S., Galtier, P., Oswald, I. & Delaforge, M. 2005. Byssochlamys nivea as a source of mycophenolic acid. App. Environ. Microbiol. 71 (1): 550-553. doi: 10.1128/AEM.71.1.550-553.2005.

Rashedi, M., Hamid, R., Mohammad, A., Hamed, A. & Ebrahim, R. 2012. Zearalenone contamination in barley, corn, silage and wheat bran. Toxicol. Ind. Health. 28 (9): 779–82. doi: 10.4236/as.2013.412084.

Rasmussen, P., Nielsen, K., Ghorbani, F., Spliid, N., Nielsen, G. & Jørgensen L. 2012. Ocurrence of differente tricothecenes and deoxynivalenol-3--D-glucoside in naturally and artificially contaminated Danish cereal grains and whole maize plants. Mycotoxin Res. 28 (3): 181-190. doi: 10.1007/s12550-012-0133-z.

Reyes, W., Isaías, S., Rojo, F., Jimenez, C., De Lucas, E., Hernández, J. & Ramírez, A. 2008. Occurrence of fungi and mycotoxins in corn silage, Jalisco State, Mexico. Rev. Iberoam. Micol. 25 (3): 182-185.

Roigé, M., Aranguren, S., Riccio, M., Pereyra, S., Soraci, A. & Tapia, M. 2009. Mycobiota and mycotoxins in fermented feed, wheat grains and corn grains in Southeastern Buenos Aires Province, Argentina. Rev. Iberoam. Micol. 26 (4): 233-237. doi: 10.1016/j.riam.2009.03.003.

Roine, K., Korpinen, E. & Kallela, K. 1971. Mycotoxicosis as a probable cause of infertility in dairy cows. Nord Vet Med. 23: 628-633.

Seeling K., Dänicke, S., Ueberschär, K., Lebzien, P. & Flachowsky, G. 2005. On the effects of Fusarium toxin-contaminated wheat and the feed intake level on the metabolism and carry over of zearalenone in dairy cows. Food Add Cont. 22 (9): 847-855.

Shimshoni, J., Cuneah, O., Sulyok, M., Krska, M., Galon, R., Sharir, N. & Shlosberg, A. Mycotoxins in corn and wheat silage in Israel. Food Add Cont. 30 (9): 1614-1625. doi: 10.1080/19440049.2013.802840.

Skladanka, J., Adam, V., Dolezal, P., Nedelnik, J., Kizek, R., Linduskova, H., Alba, J. & Nawrath, A. 2013. How Do Grass Species, Season and Ensiling Influence Mycotoxin Content in Forage?. Int. J. Environ. Res. Public Health. 10 (11): 6084-6095. doi: 10.3390/ijerph10116084.

Skladanka, J., Nedelnik, J., Adam, V., Dolezal, P., Moravcova, H. & Dohnal, V. 2011. Forage as a Primary Source of Mycotoxins in Animal Diets. Int. J. Environ. Res. Public Health. 8 (1): 37-50. doi: 10.3390/ijerph8010037.

Smith, G. 2012. Fumonisins. P 1206. In: R. Gupta (ed). Veterinary Toxicology. Ed.. 2ª edición. Elsiever. Oxford, Estados Unidos.

Storm, I., Kristensen, K., Raun, B., Smedsgaard, J. & Thrane, U. 2010. Dynamics in the microbiology of maize silage during whole-season storage. J. Appl. Microbiol. 109 (3): 1017-1026. doi: 10.1111/j.1365-2672.2010.04729.x.

Streit, E., Schwab, C., Sulyok, M., Naehrer, K., Krska, R. & Schatzmayr, G. 2013. Multi-Mycotoxin Screening Reveals the Occurrence of 139 Different Secondary Metabolites in Feed and Feed Ingredients. Toxins. 5: 504-523. doi: 10.3390/toxins5030504.

Suzuki, S., Satoh, T. & Yamazaki, M. 1977. The pharmacokinetics of ochratoxin A in rats. Jpn J Pharmacol. 27: 735-744. doi: 10.1254/jjp.27.735.

Tobía, C., Rojas, A., Villalobos, E., Soto, H. & Uribe, L. 2004. Sustitución parcial del alimento balanceado por ensilaje de soya y su efecto en la producción y calidad de la leche de vaca, en el trópico húmedo de Costa Rica. Agronomía Costarricense. 28 (2): 27-35.

Uegaki, R., Kobayashi, H., Inoue, H., Tohno, M. & Tsukiboshi, T. 2013 (a). Changes in fumonisin production in rice grain during ensiling. Anim. Sci. J. 84 (1): 48-53. doi: 10.1111/j.1740-0929.2012.01028.x.

Uegaki, R., Tsukiboshi, T. & Tohno, M. 2013 (b). Changes in the concentration of fumonisin, deoxynivalenol and Zearalenone in corn silage during ensilage. Anim. Sci. J. 84 (9): 656-662. doi: 10.1111/asj.12053.

Upadhaya, S., Park, M. & Jong, K. 2010. Mycotoxins and their biotransformation in the rumen. Asian-Aust J Anim Sci. 23 (9): 1250-1260. doi: 10.5713/ajas.2010.r.06.

Van Asselt, E., Azambuja, W., Kastelein, P., De Rijk, T., Stratakou, I. & Van Der Fels-Klerx, H. 2012. A Dutch field survey on fungal infection and mycotoxin concentrations in maize. Food Add. Cont. 29 (10): 1556-1565. doi: 10.1080/19440049.2012.689997.

Vandenbroucke, V., Croubels, S., Verbrugghe, E., Boyen, F., De Backer, P., Ducatelle, R., Rychlik, I., Haesebrouck, F. & Pasmans, F. The mycotoxin deoxynivalenol promotes uptake of Salmonella Typhimurium in porcine macrophages, associated with ERK1/2 induced cytoskeleton reorganization. Vet Res. 40 (6):64. doi: 10.1051/vetres/2009045.

Ványi, A., Szemerédi, G. & Szailer, E. 1974. Fusariotoxicosis in a cattle farm. Magy Állatorv Lapja. 29: 544-546.

Weaver, G., Kurtz, H., Behrens, J., Robison, T., Seguin, B., Bates, F. & Mirocha, C. 1986. Effect of zearalenone on dairy cows. Am. J. Vet. Res. 47 (8): 1826-1828.

Wilkinson, J. 1999. Silage and animal health. Nat. Toxins. 7 (6): 221-232. doi: 10.1002/1522-7189(199911/12)7:6<221::AID-NT76>3.0.CO;2-H.

Wu, F., Bhatnagar, D., Bui-klimke, T., Carbone, I., Hellmich, R., Munkvold, G., Paul, P., Payne, G. & Tackle E. 2011. Climate change impacts on mycotoxins risk in US maize. World Mycot J. 4 (1): 79-93. doi: 10.3920/WMJ2010.1246.

Publicado
2016-02-15
Cómo citar
Alpízar Solís, C. (2016). Presencia de hongos y contaminación con micotoxinas en ensilajes para alimentación de rumiantes. Artículo de Revisión. Ciencias Veterinarias, 33(1), 7-31. https://doi.org/10.15359/rcv.33-1.1
Sección
Artículos -sección arbitrada, pares doble ciego-