Effect of Aflatoxins in Aquaculture: Use of Bentonite Clays as Promising Remedy

Aflatoxins are among all known mycotoxins, the most widespread source of contamination of food and feed throughoutthe world. In aquaculture and aqua-feed formulations the increased use of plant based materials has intensified the risks ofaflatoxicosis in farmed fish because of the high load of aflatoxin by the vegetable sources. The aflatoxins production by toxicfungal strains can take place in the field directly, during different processing stages like insiling, aqua feed formulation,preparation and due to improper feed storage. However, the thermal treatments can only destroy the fungus but have no effecton the heat-resistant mycotoxins present in mycelium and spores of the mold. So, the aflatoxin accumulation in fish meal andfish feed represents a great threat for the aqua-cultured species and ultimately for the consumer’s health and safety.Consequently, the issue of aflatoxin contamination in fish and aquaculture industry has intensified. This review focused on thedeleterious effects of aflatoxins in fish and aquaculture and the possible remedy by the use of adsorbents.

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Abdelhamid, A. M., Abdelkhalek, A. E., Mehrm, A. I., & Khalil, F. F. (2004). An attempt to alleviate aflatoxicosis on Nile tilapia fish by dietary supplementations with chicken-hatchery by-products (egg shells) and shrimp processing wastes (shrimp shells) 2-On clinical, blood and histological parameters. Journal of Agricultural Science, 29, 6175- 6196.

Abdel-Wahhab, M. A., & Aly, S. E. (2005). Antioxidant property of nagilia sativa (black cumin) and syzygium aromaticum (clove) in rats during aflatoxicosis. Journal of Applied Toxicology, 25 (3), 218-223. https://doi.org/10.1002/jat.1057

Abdel-Wahhab, M.A., Nada, S.A., & Khalil, F.A. (2002). Physiological and toxicological responses in rats fed aflatoxin-contaminated diet with or without sorbent materials. Animal Feed Science and Technology, 97 (3), 209-219. https://doi.org/10.1016/S0377- 8401(01)00342-X

Agag, B. I. (2004). Mycotoxins in foods and feeds. Assiut University Bulletin for Environmental Researches, 7, 173-206.

Alinezhad, S., Tolouee, M., Kamalzadeh, A., Motalebi, A. A., Nazeri, M., Yasemi, M., Shams-Ghahfarokhi, M., Tolouei, R., & Razzaghi-Abyaneh, M. (2011). Mycobiota and aflatoxin B1 contamination of rainbow trout (Oncorhinchus mykiss) feed with emphasis to Aspergillus flavis. Iranian Journal of Fisheries Sciences, 10 (3), 363-374.

Almeida, J. (2013). Identification of mechanisms of beneficial effects of dietary clays in pigs and chicks during an enteric infection (PhD thesis). University of Illinois at Urbana-Champaign. USA.

Aye, P.P., Morishita, T.Y., Saif, Y.M., Latshaw, J.D., Harr, B.S., & Cihla, F. B. 2000. Induction of vitamin A deficiency in turkeys. Avian Diseases, 44, 9-17.

Ayyat, M.S., Abd-Rhman, G.A., El-Marakby, H.I., Mahmoud, H.K., & Hessan, A. A. A. (2013). Reduction the aflatoxin toxicity in Nile tilapia fish. Egyptian Journal of Nutrition and Feeds, 16, 469- 479.

Bankole, S.A., Adenusi, A. A., Lawal, O. S., & Adesanya, O.O. (2010). Occurrence of aflatoxin B1 in food products derivable from ‘egusi’ melon seeds consumed in southwestern Nigeria. Food Control, 21, 974-976. https://doi.org/10.1016/j.foodcont.2009.11.014

Barbosa, T., Pereyra, C., Soleiro, C., Dias, E., Oliveira, A., Keller, K., Silva, P., Cavaglieri, L., & Rosa, C. (2013). Mycobiota and mycotoxins present in finished fish feeds from farms in the Rio de Janeiro State, Brazil. International Aquatic Research, 5, 1-9. doi: 10.1186/2008-6970-5-3

Binder, E. M., Tan, L. M., Chin, L. J., Handle, J., & Richard, J. (2007). Worldwide occurrence of mycotoxins in commodities feed and feed ingredients. Animal Feed Science and Technology, 137, 265-282. https://doi.org/10.1016/j.anifeedsci.2007.06.005

Bintvihok, A., Thiengnin, S., Doi, K., & Kumagai, S. (2002). Residues of aflatoxins in the liver, muscle and eggs of domestic fowls. Journal of Veterinary Medical Science, 64, 1037-1039. https://doi.org/10.1292/jvms.64.1037

Cagauan, A.G., Tayaban, R.H., Somga, J.R., & Bartolome, R.M. (2004). Effect of aflatoxin contaminated feeds in Nile tilapia (Oreochromis niloticus L.). In: Remedios, R.B., Mair, G.C., Fitzsimmons, K. (Eds.), Proceedings of the Sixth International Symposium on Tilapia in Aquaculture, 172-178 pp.

Chavez-Sanchez, M.C., Palacios, C.A.M., & Moreno, I.O. (1994). Pathological effects of feeding young Oreochromis niloticus diets supplemented with different levels of Aflatoxin B1. Aquaculture, 127, 49- 60. https://doi.org/10.1016/0044-8486(94)90191-0

Dalloul, R.A., Lillehoj, H.S., Shellem, T.A., & Doerr, J.A. (2002). Effect of vitamin A deficiency on host intestinal immune response to Eimeria acervulina in broiler chickens. Poultry Science, 81, 1509-1515. https://doi.org/10.1093/ps/81.10.1509

Deng, S.X., Tian, L.X., Liu, F.J., Jin, S.J., Liang, G.Y., Yang, H.J., Du, Z.Y., & Liu, Y. J. (2010). Toxic effects and residue of aflatoxin B1 in tilapia (Oreochromis niloticus) (O. aureus) during long-term dietary exposure. Aquaculture, 307, 233-240. https://doi.org/10.1016/j.aquaculture.2010.07.029

Ding, X.X., Li, P.W., Bai, Y.Z., & Zhou, H.Y. (2012). Aflatoxin B1 in post-harvest peanuts and dietary risk in China. Food Control, 23, 143-148. https://doi.org/10.1016/j.foodcont.2011.06.026

El-Banna, R., Teleb, H.M., Hadi, M.M., & Fakhry, F.M. (1992). Performance and tissue residue of tilapias fed dietary aflatoxin. Journal of Veterinary Medicine, 40, 17-23.

El-Boshy, M. E., El-Ashram, A. M. M., & El-Ghany, N. A. A. (2008). Effect of dietary β-1, 3 glucan on immunomodulation on diseased Oreochromis niloticus experimentally infected with aflatoxin. 8th International Symposium on Tilapia in Aquaculture, Cairo, Egypt, October, 2008, 12-14 pp.

El-Enbaawy, M., Adel, M., Marzouk, M.S., & Salem, A. A. (1994). The effects of acute and chronic aflatoxicosis on the immune functions of Oreochromis niloticus in Egypt. Veterinary Medical Journal Giza, 42, 47-52.

Ellis, R.W., Clements, M., Tibbetts, A., & Winfree, R. (2000). Reduction of the bioavailability of 20 mg/kg aflatoxin in trout feed containing clay. Aquaculture, 183, 179-188. https://doi.org/10.1016/S0044- 8486(99)00292-6

El-Sayed, Y.S., & Khalil, R.H. (2009). Toxicity, biochemical effects and residue of aflatoxin B1 in marine water reared sea bass (Dicentrarchus labrax). Food and Chemical Toxicology, 47, 1606-1609. https://doi.org/10.1016/j.fct.2009.04.008

Encarnacao, P., Srikhum, B., Rodrigues, I., & Hofstetter, U. (2009). Growth performance of red tilapia (O. niloticus x O. mossambicus) fed diets contaminated with aflatoxin B1 and the use of a commercial product to suppress negative effects. Book of abstracts, World Aquaculture 2009, Veracruz, Mexico.

Farabi, S.M., Yousefian, M., & Hajimoradloo, A. (2006). Aflatoxicosis in juvenile Huso huso fed Aflatoxin-B1 contaminated diet. Journal of Applied Ichthyology, 22, 234-237. https://doi.org/10.1111/j.1439- 0426.2007.00958.x

Glahn, R., Beers, K., Bottje, W., Wideman, R.J., Huff, W., & Thomas, W. (1991). Aflatoxicosis alters avian renal function, calcium, and vitamin D metabolism. The Journal of Toxicology and Environmental Health, 34, 309-321. https://doi.org/10.1080/15287399109531570

Groopman, J.D., Wang, J.S., & Scholl, P. (1996). Molecular biomarkers for aflatoxins: from adducts to gene mutations to human liver cancer. Canadian Journal of Physiology and Pharmacology, 74, 203- 209. https://doi.org/10.1139/y96-009

Han, D., Xie, S., Zhu, X., Yang, Y., & Guo, Z. (2010). Growth and hepatopancreas performances of gibel carp fed diets containing low levels of aflatoxin B1. Aquaculture Nutrition, 16, 335-342. https://doi.org/10.1111/j.1365-2095.2009.00669.x

Hassan, A.M., Kenawy, A.M., Abbas, W.T., & AbdelWahhab, M.A. (2010). Prevention of cytogenetic, histochemical and biochemical alterations in Oreochromis niloticus by dietary supplement of sorbent materials. Ecotoxicology and Environmental Safety, 73, 1890-1895. https://doi.org/10.1016/j.ecoenv.2010.07.041

Hauptman, B.S., Barrows, F.T., Block, S.S., Gaylord, T.G., Paterson, J.A., & Sealey, W.M. (2014). Potential for a Mycotoxin Deactivator to Improve Growth and Performance of Rainbow Trout fed High Levels of an Ethanol Industry Co-Product, Grain Distiller's Dried Yeast. North American Journal of Aquaculture, 76, 297-304. https://doi.org/10.1080/15222055.2014.902891

Hoover, G. J., El-Mowafi, A., Simko, E., Kocal, T.E., Ferguson, H.W., & Hayes, M.A. (1998). Plasma proteins of rainbow trout Oncorhynchus mykiss isolated by binding to lipopolysaccharide from Aeromonas salmonicida. Comparative Biochemistry and physiology part B: biochemistry and molecular biology, 1998. 120, 559-569.

Hu, C.H., Xu, Y., Xia, M.S., Xiong, L., & Xu, Z.R. (2008). Effects of Cu2+ -exchange montmorillonite on intestinal microflora, digestibility and digestive enzyme activities of Nile tilapia. Aquaculture Nutrition, 14, 281-288. https://doi.org/10.1111/j.1365- 2095.2007.00531.x

Huang, Y., Han, D.X., Zhu, M., Yang, Y.X., Jin, J.Y., Chen, Y.F., & Xie. S.Q. (2011). Response and recovery of gibel carp from subchronic oral administration of aflatoxin B1. Aquaculture, 319, 89- 97. https://doi.org/10.1016/j.aquaculture.2011.06.024

Hussain, D., Mateen, A., & Gatlin, D.M. III. (2017). Alleviation of aflatoxin B1 (AFB1) toxicity by calcium bentonite clay: Effects on growth performance, condition indices and bioaccumulation of AFB1 residues in Nile tilapia (Oreochromis niloticus). Aquaculture, 475, 8-15. https://doi.org/10.1016/j.aquaculture.2017.04.003

Huwig, A., Freimund, S., Kappeli, O., & Dutler, H. (2001). Mycotoxin detoxification of animal feed by different adsorbents. Toxicology Letters, 122, 179188. https://doi.org/10.1016/S0378-4274(01)00360-5

Jantrarotai, I.V., & Lovell, R.T. (1990). Sub chronic toxicity of dietary aflatoxin B1 to channel catfish. Journal of Aquatic Animal Health, 2, 248-254. https://doi.org/10.1577/1548- 8667(1990)002<0248:STODAB>2.3.CO;2

Jaynes, W.F., & Zartman, R.E. (2011). Aflatoxin Toxicity Reduction in Feed by Enhanced Binding to SurfaceModified Clay Additives. Toxin, 3, 551-565. doi:10.3390/toxins3060551

Kannewischer, I., Arvide, M.G.T., White, G.N., & Dixon, J.B. (2006). Smectite clays as adsorbents of aflatoxin B1 initial steps. Clay Science, 12, 199-204.

Kenawy, A.M., El-Genaidy, H.M. Authman, M.M.N., & Abdel-Wahhab, M.A. (2009). Pathological studies on effects of aflatoxin on Oreochromis niloticus with application of different trials of control. Egyptian Journal of Comparative Pathology and Clinical Pathology, 22, 175-193.

Lindemann, M.D., Blodgett, D.J. Kornegay, E.T., & Schuryg, G.G. (1993). Potential ameliorators of aflatoxicosis in weanling growing swine. Journal of Animal Science, 71, 171-178. https://doi.org/10.2527/1993.711171x

Manning, B.B., Li, M.H., & Robinson, E.H. (2005). Aflatoxins from mouldy corn causes no reductions in channel catfish Ictalurus punctatus performance. The Journal of the World Aquaculture Society, 36, 59-67. https://doi.org/10.1111/j.1749-7345.2005.tb00131.x

Mayura, K., Abdel-Wahhab, M.A., McKenzie, K.S., Sarr, A.B., Edwards, J.F., Naguib, K., & Phillips, T.D. (1998). Prevention of maternal and developmental toxicity in rats via dietary inclusion of common aflatoxin sorbents: potential for hidden risks. Toxicological Sciences, 41, 175-182. https://doi.org/10.1093/toxsci/41.2.175

Mehrim, A.I., & Salem, M.F. (2013). Medicinal herbs against aflatoxicosis in Nile tilapia (Oreochromis niloticus): Clinical signs, postmortem lesions and liver histopathological changes. Egyptian Journal of aquaculture, 3, 13-25.

Meissonnier, G.M., Laffitte, J., Loiseau, N., Benoit, E., Raymond, I., Pinton, P., Cossalter, A.M. Bertin, G., Oswald, I.P., & Galtier, P. (2007). Selective impairment of drug metabolizing enzymes in pig liver during subchronic dietary exposure to aflatoxin B1. Food and Chemical Toxicology, 45, 2145-2154. https://doi.org/10.1016/j.fct.2007.05.012

Nomura, H., Ogiso, M., Yamashita, M., Takaku, H.H., Kimura, A., Chikasou, M., Nakamura, Y., Fujii, S., Watai, M.Y., & Amada, H. (2011). Uptake by dietary exposure and elimination of aflatoxins 35 in muscle and liver of rainbow trout (Oncorhynchus mykiss). Journal of Agricultural and Food Chemistry, 59, 5150-5158. DOI: 10.1021/jf1047354

Nunes, E.M.C.G., Pereira, M.M.G., Costa, A.P.R., Rosa, C.A.D.A., Pereyra, C.M., Calvet, R.M., Marques, A.L.A., Filho, F.D.C.C., & Muratori, M.C.S. (2015). Screening of aflatoxin B1 and mycobiota related to raw materials and finished feed destined for fish. Latin American Journal of Aquatic Research, 43, 595- 600.

Ok, H.E., Kim, H.J., Shim, W.B., Lee, H., Bae, D.H., & Chung, D.H. (2007). Natural occurrence of aflatoxin B1 in the marketed foods and risk estimates of dietary exposure in Koreans. Journal of Food Protection, 70, 2824-2828. https://doi.org/10.4315/0362-028X70.12.2824

Ottinger, C.A., & Kaattari, S.L. (2000). Long-term immune dysfuntion in rainbow trout (Oncorhynchus mykiss) exposed as embryos to aflatoxin B1. Fish and Shellfish Immunology, 10, 101-106. https://doi.org/10.1006/fsim.1999.0227

Phillips, T.D. (1999). Dietary clay in the chemoprevention of aflatoxin induced disease", Toxicological Sciences, 52, 118-126. https://doi.org/10.1093/toxsci/52.suppl_1.118

Phillips, T.D., Kubena, L.F., Harvey, R.B., Taylor, D.R., & Heidelbaugh, N.D. (1988). Hydrated sodium calcium aluminosilicate: a high affinity sorbent for aflatoxin. Poultry Science, 67, 243-247. https://doi.org/10.3382/ps.0670243

Phillips, T.D., Lemke, S.L., & Grant, P.G. (2002). Characterization of clay-based enterosorbents for the prevention of aflatoxicosis. Advances in Experimental Medicine and Biology, 504, 157-71.

Pier, A. C. (1986). Immunomodulation in aflatoxicosis. Diagnosis of mycotoxicoses, 143-148 pp.

Pimpukdee, K., Kubena, L.F., Bailey, C.A., Huebner, H.J., Afriyie-Gyawu, E., & Phillips, T. D. (2004). Aflatoxin-induced toxicity and depletion of hepatic vitamin A in young broiler chicks: Protection of chicks in the presence of low levels of NovaSil PLUS in the diet. Poultry Science, 83,737-744.

Puschner, B. (2002). Mycotoxins. Veterinary Clinics of North America: Small Animal Practice, 32, 409-419. Raghavan, P.R., Zhu, X., Lei, W., Han, D., Yang, Y., &

Xie, S. (2011). Low levels of aflatoxin B1 could cause mortalities in juvenile hybrid sturgeon, Acipenser ruthenus♀ × A. baerii♂. Aquaculture Nutrition, 13, 39-47. doi.org/10.1111/j.1365-2095.2009.00725.x

Ruby, D.S., Masood, A., & Fatmi, A. (2013). Effect of Aflatoxin Contaminated Feed on Growth and Survival of Fish Labeo Rohita (Hamilton). Current World Environment Journal, 8, 479-482. DOI: http://dx.doi.org/10.12944/CWE.8.3.19

Sahoo, P.K., & Mukherjee, S.C. (2001). Effect of dietary β1, 3 glucan on immune responses and disease resistance of healthy and aflatoxin B1-induced immune compromised rohu (Labeo rohita Hamilton). Fish Shellfish Immunology, 11, 683-695. https://doi.org/10.1006/fsim.2001.0345

Salem, M.F.I., Shehab, E.M.T., Khalafallah, M.M.M.A., Sayed, S.H., & Amal, S.H. (2010). Nutritional Attempts to Detoxify Aflatoxic Effects in Diets of Tilapia Fish (Oreochromis niloticus). The Journal of the World Aquaculture Society, 5, 195-206.

Santacroce, M.P., Conversano, M.C., Casalino, E., Lai, O., Zizzadoro, C., Centoducati, G., & Crescenzo, G. (2008). Aflatoxins in aquatic species: metabolism, toxicity and perspectives. Reviews in Fish Biology and Fisheries, 18, 99-130. https://doi.org/10.1007/s11160-007-9064-8

Santacroce, M.P., Narracci, M. Acquaviva, M.I., Cavallo, R.A., Zacchino, V., & Centoducati, G. (2011). New development in aflatoxin research: from aquafeed to marine cells. In Irineo Torres-Pacheco, I. Eds., Aflatoxins-Detection, Measurement and Control, Publisher In Tech, Croatia. 209-234 pp.

Selim K.M., Elhofy, H., & Khalil, R.H. (2013). The efficacy of three mycotoxin adsorbents to alleviate afla toxin B1 induced toxicity in Oreochromis niloticus. Aquaculture International, 22, 523-540. DOI 10.1007/s10499-013-9661-6

Sepahdari, A., Ebrahimzadeh, M., Sharifpour, H.A.I., Khosravi, A., Motallebi, A.A., Mohseni, S., Kakoolaki, M., Pourali, H.R., & Hallajian, A. (2010). Effects of different dietary levels of Aflatoxin B1 on survival rate and growth factors of Beluga (Huso huso). Iranian Journal of Fisheries Sciences, 9, 141- 150.

Soubra, L., Sarkis, D. Hilan, C., & Verger, P. (2009). Occurrence of total aflatoxins, ochratoxin A and deoxynivalenol in foodstuffs available on the Lebanese market and their impact on dietary exposure of children and teenagers in Beirut. Food Additives and Contaminants, 26, 189-200. https://doi.org/10.1080/02652030802366108

Tacon, A.G.J., & Metian, M. (2008). Global overview on the use of fish meal and fish oil in industrially compounded aquefeeds: trends and future prospect. Aquaculture, 285, 146-158. doi:10.1016/j.aquaculture.2008.08.015

Tomasevic-canovic, M., Dakovic, A., & Markovic, V. (2001). The effect of exchangeable cations in clinoptilolite and montmorillonite on the adsorption of aflatoxin B1. Journal of the Serbian Chemical Society, 66, 555-561.

Tuan, N.A., Manning, B.B., Lovell, R.T., & Rottinghaus, G. E. (2002). Response of Nile tilapia (Oreochromisniloticus) fed diets containing different concentrations of moniliformin or fumonisin B1. Aquaculture, 217, 515-528. https://doi.org/10.1016/S0044-8486(02)00021-2

Varior, S., & Philip, B. (2012). Aflatoxin B1 induced alterations in the stability of the lysosomal membrane in Oreochromis mossambicus (Peters 1852). Aquaculture Research, 43, 1170-1175. https://doi.org/10.1111/j.1365-2109.2011.02920.x

Velazquez, A.L.B., Bailey, C.A., Deng, Y., & Dixon, J.B. (2010). Evaluation of Bentonites as an Amendment in Poultry Feed Contaminated with High-Concentration of Aflatoxins. In: SEA-CSSJ-CMS Trilateral Meeting On Clays. June 8-10, 2010 Seville, Spain.

Zychowski, K.E., Hoffman, A.R., Ly, H.J., Pohlenz, C., Buentello, A., Romoser, A., Gtalin, D. M., & Philips, T.D. (2013a). The Effect of Aflatoxin-B1 on Red Drum (Sciaenops ocellatus) and Assessment of Dietary Supplementation of NovaSil for the Prevention of Aflatoxicosis. Toxins, 5, 1555-1573. https://doi.org/10.3390/toxins5091555

Zychowski, K.E., Pohlenz, C., Mays, T., Romoser, A., Hume, M., Buentello, A., Gatlin, D.M., & Phillips, T.D. (2013b). The effect of NovaSil dietary supplementation on the growth and health performance of Nile tilapia (Oreochromis niloticus) fed aflatoxin-B1 contaminated feed. Aquaculture, 76, 117-123. https://doi.org/10.1016/j.aquaculture.2012.11.020
Turkish Journal of Fisheries and Aquatic Sciences-Cover
  • ISSN: 1303-2712
  • Başlangıç: 2015
  • Yayıncı: Su Ürünleri Merkez Araştırma Enstitüsü - Trabzon
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