The effects of low levels of aflatoxin B1 on health, growth performance and reproductivity in male rabbits


  • Yawang Sun Southwest University
  • Guozhong Dong Southwest University
  • Guangxin E Southwest University
  • Min Liao Southwest University
  • Lin Tao Southwest University
  • Jingzhi Lv Southwest University



rabbits, aflatoxin, growth performance, immune function, reproductivity


This study investigated the chronic effects of relatively low exposure to aflatoxin B1 (AFB1) on the growth performance, immune situation and reproduction in male rabbits. Bucks (n=32, 4.82±0.22 kg) were individually assigned to 4 treatments (8 replicates each) using a randomised complete block design. Four diets containing 0, 0.02, 0.05, and 0.1 mg AFB1/kg, were provided to bucks for 8 wk. Growth performance and semen quality were measured. Blood, organ and tissue samples were collected to measure haematological indices, liver function, organ weights and immune parameters. Compared to control, AFB1-contaminated diets reduced body weight and average daily gain (P<0.05), altered certain haematological indices and liver function with decreased monocytes percentage and mean corpuscular haemoglobin concentration, and increased plateletcrit and albumin (P<0.05), slightly impaired reproductive parameters with enhanced ratio of morphologically abnormal sperm cells at early stage and reduced post-stage acrosome integrity, testis weight and serum testosterone concentration (P<0.05), decreased immune function with reduced relative liver weight (%) and tumour necrosis factor-α levels in serum and liver tissue, and increased serum 8-hydroxy-2’-deoxyguanosine levels (P<0.05). Furthermore, bucks fed diets with relatively high AFB1 (0.05 and 0.1 mg AFB1/kg) had reduced red blood cell and haematocrit (P<0.05) in contrast with the low AFB1 group (0.02 mg AFB1/kg). In conclusion, diets containing 0.05 and 0.1 mg AFB1/kg had negative effects on bucks’ growth performance, haematology, reproductivity and immune function, whereas diet containing 0.02 mg AFB1/kg had only minor effects on the parameters measured.


Download data is not yet available.

Author Biographies

Yawang Sun, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation

Guozhong Dong, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation

Guangxin E, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation

Min Liao, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation

Lin Tao, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation

Jingzhi Lv, Southwest University

Chongqing Engineering Research Center for Herbivores Resource Protection and Utilisation


Abdelaziz S.A., Hamada M.M. 2007. Phytic acid exposure alters AflatoxinB1-induced reproductive and oxidative toxicity in Albino Rats (Rattus norvegicus). eCAM, 6: 331-3471.

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 Sci. Tech., 97: 209-219.

Abnet C.C. 2007.Carcinogenic food contaminants. Cancer Invest., 25: 189-196.

Adedara I.A., Nanjappa M.K., Farombi E.O., Akingbemi B.T. 2014. Aflatoxin B1 disrupts the androgen biosynthetic pathway in rat Leydig cells. Food Chem. Toxicol., 65: 252-259.

Alm K., Dahlbom M., Saynajarvi M., Anderson M.A., Salkinoja-Salonen M.S., Anderson M.C. 2002. Impaired semen quality of AI bulls fed with moldy hay: a case report. Theriogenology, 58: 1497-1502.

Asare G.A., Bronz M., Naidoo V., Kew M.C. 2007. Interactions between aflatoxin B1 and dietary iron overload in hepatic mutagenesis. Toxicol., 234: 157-166.

Ataman M.B., Dönmez H.H., Dönmez N., Sur E., Bucak M.N., Çoyan, K. 2014. Protective effect of esterified glucomannan on aflatoxin-induced changes in testicular function, sperm quality, and seminal plasma biochemistry in rams. Theriogenology, 81: 373-380.

Clarke R.N., Doerr J.A., Ottinger M.A. 1986. Relative importance of dietary aflatoxin and feed restriction on reproductive changes associated with aflatoxicosis in the maturing white leghorn male. Poul. Sci., 65: 2239-2245.

Cotty P.J., Jaime-Garcia R. 2007. Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int. J. Food Microbiol., 199: 109-115.

David S.S., O’Shea V.L., Kundu S. 2007. Base-excision repair of oxidative DNA damage. Nature, 447: 941-950.

Dönmez N., Keskin E. 2008. The effects of aflatoxin and glucomannan on some antioxidants and biochemical parameters in rabbits. Acta Vet. Beograd., 58: 307-313.

Egbunike G.N. 1982. Steroidogenic and spermatogenic potentials of the male rat after acute treatment with Aflatoxin B1. Andrologia, 14: 440-446.

Eisa A.M.A., Metwally A.Y. 2011. Effect of glucomannan on haematological, coagulation and biochemical parameters in male rabbits fed aflatoxin-contaminated ration. World Mycotoxin J., 4: 183-188.

Ellis O., Smith J.P., Simpson B.K. 1991. Aflatoxins in food: occurrence, biosynthesis, effects on organisms, detection, and methods of control. Crit. Rev. Food. Sci., 30: 403-439.

European Commission. 2003. Commission directive 2003/100/EC of 31 October 2003 amending Annex I to Directive 2002/32/EC of the European Parliament and of the Council on undesirable substances in animal feed. No. 2003/100/EC, 31 October 2003. Off. J. Eur. Comm., 1 November 2003, L 285, 33-37.

Ewuola E.O. 2008. Organ traits and histopathology of rabbits fed varied levels of dietary fumonisin B1. J. Anim. Physiol. An. N., 93: 726-731.

Ewuola E.O., Egbunike G.N. 2010. Effects of dietary fumonisin B1 on the onset of puberty, semen quality, fertility rates and testicular morphology in male rabbits. Reproduction, 139: 439-445.

Ewuola E.O., Jimoh O.A., Bello A.D., Bolarinwa A.O. 2014. Testicular biochemicals, sperm reserves and daily sperm production of West African dwarf bucks fed varied levels of dietary aflatoxin. Anim. Reprod. Sci., 148: 182-187.

Fan Y., Li X., Zhao L., Jia Y., Ji C., Ma Q., Chen Y., Wang L. 2012. Investigation on contamination situation of aflatoxin in detected feeds and feedstuffs in Beijing area. Scientia Agricultura Sinica, 45: 5102-5109.

Fan Y., Zhao L., Ma Q., Li X., Shi H., Zhou T., Zhang J., Ji C. 2013. Effects of Bacillus subtilis ANSB060 on growth performance, meat quality and aflatoxin residues in broilers fed moldy peanut meal naturally contaminated with aflatoxins. Food Chem. Toxicol., 59: 748-753.

Faridha A., Faisal K., Akbarsha M.A. 2006. Duration-dependent histopathological and histometric changes in the testis of aflatoxin-treated mice. J. Endocrin. Reprod., 10: 117-133.

Gholami-Ahangaran M., Zia-Jahromi N. 2013. Nanosilver effects on growth parameters in experimental aflatoxicosis in broiler chickens. Toxicol. Ind. Health, 29: 121-125.

Gong Y., Hounsa A., Egal S., Turner P.C., Sutcliffe A.E., Hall A.J., Cardwell K., Wild C.P. 2004. Post-weaning exposure to aflatoxin results in impaired child growth: a longitudinal study in Benin. Environ. Health Perspect., 112: 1334-1338.

Guerre P., Eeckhoutte C., Larrieu G., Burgat V., Galtier P. 1996. Dose-related effect of aflatoxin B1 on liver drug metabolizing enzymes in rabbit. Toxicology, 108: 39-48.

Guerre P., Larrieu G., Burgat V., Galtier P. 1999. Cytochrome P450 decreases are correlated to increased microsomal oxidative damage in rabbit liver and primary cultures of rabbit hepatocytes exposed to AFB1. Toxicol. Lett., 104: 117-125.

Guindon-Kezis K.A., Mulder J.E., Massey T.E. 2014. In vivo treatment with aflatoxin B1 increases DNA oxidation, base excision repair activity and 8-oxoguanine DNA glycosylase 1 levels in mouse lung. Toxicology, 321: 21-26.

Hancock K.D., Coleman E.S., Tao Y.X., Morrison E.E., Braden T.D., Kemppainen B.W., Akingbemi B.T. 2009. Genistein decreases androgen biosynthesis in rat Leydig cells by interference with luteinizing hormone-dependent signaling. Toxicol. Lett., 184: 169-175.

Issac A.A., Manjunatha K.N., Ebenezer O.F., Benson T.A. 2014. Aflatoxin B1 disrupts the androgen biosynthetic pathway in rat Leydig cells. Food Chem. Toxicol., 65: 252-259.

Kaneko J.J., Harvey J.W., Bruss M. 1997. Serum protein and the dysproteinemias. In clinical biochemistry of domestic animals, 5th ed.; Academic press: San Diego, CA, USA; pp. 117-137.

Kärenlampi S.O. 1987. Mechanism of cytotoxicity of aflatoxin B1: role of cytochrome P1-450. Biochem. Bioph. Res. Co., 145: 845-860.

Kecici T., Demet Ö., Oguz H. 1995. Single and combined effects of dietary aflatoxin and adsorbent (Mycofix plus) on some hematological and serum biochemical parameters of broiler chickens. J. Vet. Sci., 11: 95-101.

Kovács M., Tornyos G., Matics Zs., Kametler L., Rajli V., Bodnár Zs., Kulcsár M., Huszenicza Gy., Keresztes Zs., Cseh S. 2011. Subsequent effect of subacute T-2 toxicosis on spermatozoa, seminal plasma and testosterone production in rabbits. Animal, 5: 1563-1569.

Manafi M., Murthy H.N.N., Mohan K., Narayana H.D.S. 2012. Evaluation of different mycotoxin binders on broiler breeders induced with aflatoxin B1: effects on fertility, hatchability, embryonic mortality, residues in egg and semen quality. Global Vet., 8: 643-648.

Marin D.E., TaranuI., Bunaciu R.P., Pascale F., Tudor D.S., Avram N., Sarca M., Cureu I., Criste R.D., Suta V., Oswald I.P. 2002. Changes in performance, blood parameters, humoral and cellular immune responses in weanling piglets exposed to low doses of aflatoxin. J. Anim. Sci., 80: 1250-1257.

Mohanamba T., Rao M.R., Habibi S.M.M. 2007. Aflatoxin contamination in animal feeds. Ind. Vet. J., 84:416.3

Morton D. 1988. The use of rabbits in male reproductive toxicology. Environ. Health Persp., 77: 5-9.

Oguz H., Kurtoglu V. 2000. Effect of clinoptilolite on performance of broiler chickens during experimental aflatoxicosis. Brit. Poult. Sci., 41: 512-517.

Peters L.P., Teel R.W. 2003. Effect of high sucrose diet on liver enzyme content and activity and aflatoxin B1-induced mutagenesis. InVivo.,17: 205-210.

Prabu P.C., Dwivedi P., Sharma A.K. 2013. Toxico pathological studies on the effects of aflatoxin B1, ochratoxin A and their interaction in New Zealand White rabbits. Exp. Toxicol. Pathol., 65: 277-286.

Richard J.L., Thurston J.R. 1975. Effect of aflatoxin on phagocytosis of Aspergillus fumigatus spores by rabbit alveolar macrophages. Appl. Microbiol., 30: 44-47.

Rustemeyer S.M., Lamberson W.R., Ledoux D.R., Rottinghaus G.E., Shaw D.P., Cockrum R.R., Kessler K.L., Austin K.J., Cammack K.M. 2014. Effects of dietary aflatoxin on the health and performance of growing barrows. J. Anim. Sci., 88: 3624-3630.

Salem M.H., Kamel K.I., Yousef M.I., Hassan G.A., ELNouty F.D. 2001. Protective role of ascorbic acid to enhance semen quality of rabbits treated with sublethal doses of aflatoxin B1. Toxicology, 162: 209-218.

Sherrill J.D., Sparks M., Dennis J., Mansour M., Kemppainen B.W., Bartol F.F., Morrison E.E., Akingbemi B.T. 2010. Developmental exposures of male rats to soy isoflavones impact Leydig cell differentiation. Biol. Reprod., 83: 488-501.

Soliman K.M., El-Faramawy A.A., Zakaria S.M., Mekkawy S.H. 2001. Monitoring the preventive effect of hydrogen peroxide and γ-radiation of aflatoxicosis in growing rabbits and the effect of cooking on aflatoxin residues. J. Agric. Food Chem., 49: 3291-3295.

Tung H.T., Donaldson W.E., Hamilton P.B. 1972. Altered lipid transport during aflatoxicosis. Toxicol. Appl. Pharmacol., 22: 97-104.

Verma R.J., Mathuria N. 2010. Curcumin ameliorates aflatoxininduced changes in caput and cauda epididymis of mice. Int. J. Fertil. Steril., 4: 17-22.

Waal Malefyt R., Abrams J., Bennett B., Figdor C.G., de Vries J.E. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis: An auto regulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.

Weaver A.C., See M.T., Hansen J.A., Kim Y.B, De Souza A.L.P., Teena F.M., Kim S.W. 2013. The use of feed additives to reduce the effects of aflatoxin and deoxynivalenol on pig growth, organ health and immune status during chronic exposure. Toxins, 5: 1261-1281.

Williams J.H., Phillips T.D., Jolly P.E., Stiles J.K., Jolly C.M. Aggarwal D. 2004. Human aflatoxicosis in developing countries; a review of toxicology, exposure, potential health consequences, and interventions. Am. J. Clin. Nutr., 80: 1106-1122.

Yang J., Bai F., Zhang K., Bai S., Peng X., Ding X., Li Y., Zhang J., Zhao L. 2012. Effects of feeding corn naturally contaminated with aflatoxin B1 and B2 on hepatic functions of broilers. Poul. Sci., 91: 2792-2801.

Yegani M., Smith T.K., Leeson S., Boermans H.J. 2006. Effects of feeding grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of broiler breeders. Poult. Sci., 85: 1541-1549.

Yu F.L. 1982. Studies on the mechanism of aflatoxin B1 inhibition of the rat liver nucleolar RNA synthesis. J. Biol. Chem., 256: 3292-3297.

Yunus A.W., Razzazi-Fazeli E., Bohm J. 2011. Aflatoxin B1 in affecting broiler’s performance, immunity, and gastrointestinal tract: a review of history and contemporary issues. Toxins, 3: 566-590.