Fusarium mycotoxins: Effects on reproductive function in domestic animals-A review

Theriogenology

Volumn 80, Issue 6, 2013, Pages 557-564

  Cortinovis, Cristina ^a   Pizzo, Fabiola ^a   Spicer, Leon J ^b   Caloni, Francesca ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Domestic animals; Fusarium mycotoxins; Reproductive toxicity

Indexed keywords

ANIMALIA; FUNGI; FUSARIUM; SUIDAE;

MYCOTOXIN;

ANIMAL; ANIMAL FOOD; DOMESTIC ANIMAL; DRUG EFFECT; FEMALE; FOOD CONTAMINATION; FUSARIUM; FUSARIUM MYCOTOXINS; PATHOGENICITY; PATHOPHYSIOLOGY; PREGNANCY; REPRODUCTION; REPRODUCTIVE TOXICITY; REVIEW; SWINE; SWINE DISEASE;

DOMESTIC ANIMALS; FUSARIUM MYCOTOXINS; REPRODUCTIVE TOXICITY;

ANIMAL FEED; ANIMALS; ANIMALS, DOMESTIC; FEMALE; FOOD CONTAMINATION; FUSARIUM; MYCOTOXINS; PREGNANCY; REPRODUCTION; SWINE; SWINE DISEASES;

EID: 84883053026     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2013.06.018     Document Type: Review

References (90)

1. D'Mello J.P.F., Placinta C.M., Macdonald A.M.C. Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Anim Feed Sci Technol 1999, 80:183-205.
2. Glenn A.E. Mycotoxigenic Fusarium species in animal feed. Anim Feed Sci Technol 2007, 137:213-240.
3. Mirocha C.J., Pathre S.V., Christensen C.M. Zearalenone. Mycotoxins in human and animal health 1977, 346-364. Pathotox Publisher Inc, Park Forest South, IL, USA. J.V. Rodricks, C.W. Hesseltine, M.A. Mehlman (Eds.).
4. Minervini F., Dell'Aquila M.E. Zearalenone and reproductive function in farm animals. Int J Mol Sci 2008, 9:2570-2584.
5. Chang K., Kurtz H.J., Mirocha C.J. Effects of the mycotoxin zearalenone on swine reproduction. Am J Vet Res 1979, 40:1260-1270.
6. Flowers B., Cantley T., Day B.N. A comparison of effects of zearalenone and estradiol benzoate on reproductive function during the estrous cycle in gilts. J Anim Sci 1987, 65:1576-1584.
7. Edwards S., Cantley T.C., Rottinghaus G.E., Osweiler G.D., Day B.N. The effects of zearalenone on reproduction in swine. I. The relationship between ingested zearalenone dose and anestrus in non-pregnant, sexually mature gilts. Theriogenology 1987, 28:43-49.
8. Etienne M., Jemmali M. Effects of zearalenone (F2) on estrous activity and reproduction in gilts. J Anim Sci 1982, 55:1-10.
9. Young L.G., King G.J. Low concentrations of zearalenone in diets of mature gilts. J Anim Sci 1986, 63:1191-1196.
10. Kidder H.E., Casida L.E., Grummer R.H. Some effects of estrogen injections on the estrual cycle of gilts. J Anim Sci 1955, 14:470-474.
11. Gardner M.L., First N.L., Casida L.E. Effect of exogenous estrogens on corpus luteum maintenance in gilts. J Anim Sci 1963, 22:132-134.
12. Young L.G., Ping H., King G.J. Effects of feeding zearalenone to sows on rebreeding and pregnancy. J Anim Sci 1990, 68:15-20.
13. Alm H., Greising T., Brussow K.P., Torner H., Tiemann U. The influence of the mycotoxins deoxynivalenol and zearalenol on invitro maturation of pig oocytes and invitro culture of pig zygotes. Toxicol InVitro 2002, 16:643-648.
14. Malekinejad H., Schoevers E.J., Daemen I.J.J.M., Zijstra C., Colenbrander B., Fink-Gremmels J., et al. Exposure of oocytes to the Fusarium toxins zearalenone and deoxynivalenol causes aneuploidy and abnormal embryo development in pigs. Biol Reprod 2007, 77:840-847.
15. Alm H., Brussow K.P., Torner H., Vanselow J., Tomek W., Danicke S., et al. Influence of Fusarium-toxin contaminated feed on initial quality and meiotic competence of gilt oocytes. Reprod Toxicol 2006, 22:44-50.
16. Tiemann U., Tomek W., Schneider F., Vanselow J. Effects of the mycotoxins α- and β-zearalenol on regulation of progesterone synthesis in cultured granulosa cells from porcine ovaries. Reprod Toxicol 2003, 17:673-681.
17. Ranzenigo G., Caloni F., Cremonesi F., Aad P.Y., Spicer L.J. Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells. Anim Reprod Sci 2008, 107:115-130.
18. Guthrie H.D., Bolt D.J., Cooper B.S. Changes in follicular estradiol-17 beta, progesterone and inhibin immunoactivity in healthy and atretic follicles during preovulatory maturation in the pig. Domest Anim Endocrinol 1993, 10:127-140.
19. Pan Z., Zhang J., Lin F., Ma X., Wang X., Liu H. Expression profiles of key candidate genes involved in steroidogenesis during follicular atresia in the pig ovary. Mol Biol Rep 2012, 39:10823-10832.
20. Zhu L., Yuan H., Guo C., Lu Y., Deng S., Yang Y., et al. Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3- and caspase-9-dependent mitochondrial signaling pathway. J Cell Physiol 2012, 227:1814-1820.
21. Weaver G.A., Kurtz H.J., Behrens J.C., Robison T.S., Seguin B.E., Bates F.Y., et al. Effect of zearalenone on the fertility of virgin dairy heifers. Am J Vet Res 1986, 47:1395-1397.
22. Towers N.R., Sprosen J.M. Zearalenone-induced infertility in sheep and cattle in New Zealand. N Z Vet J 1993, 41:223-224.
23. Minervini F., Dell'Aquila M.E., Maritato F., Minoia P., Visconti A. Toxic effects of the mycotoxin zearalenone and its derivatives on invitro maturation of bovine oocytes and 17β-estradiol levels in mural granulosa cell cultures. Toxicol InVitro 2001, 15:489-495.
24. Takagi M., Mukai S., Kuriyagawa T., Takagaki K., Uno S., Kokushi E., et al. Detection of zearalenone and its metabolites in naturally contaminated follicular fluids by using LC/MS/MS and invitro effects of zearalenone on oocyte maturation in cattle. Reprod Toxicol 2008, 26:164-169.
25. Pizzo F, F Caloni, N Schreiber, M Totty, and LJ Spicer. Individual and combined effects of deoxynivalenol and zearalenone on steroidogenesis in bovine granulosa cells. European Society of Toxicology InVitro 2012 International Conference, October 16-19, 2012 (Abstract.).
26. Juhasz J., Nagy P., Kulesar M., Szigeti G., Reiczigel J., Huszenicza G. Effect of low-dose zearalenone exposure on luteal function, follicular activity and uterine oedema in cycling mares. Acta Vet Hung 2001, 49:211-222.
27. Aurich J.E., Hoppen H.O., Trampler R., Zentek J., Boehm J., Razzazi-Fazeli E., et al. Effects of mycotoxins on reproductive function in mares. Anim Reprod Sci 2006, 94:238-241.
28. Minervini F., Giannoccaro A., Fornelli F., Dell'Aquila M.E., Minoia P., Visconti A. Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod Biol Endocrinol 2006, 4:62.
29. Ndossi D.G., Frizzell C., Tremoen N.H., Fæste C.K., Verhaegen S., Dahl E., et al. An invitro investigation of endocrine disrupting effects of trichothecenes deoxynivalenol (DON), T-2 and HT-2 toxins. Toxicol Lett 2012, 214:268-278.
30. Schoevers E.J., Fink-Gremmels J., Colenbrander B., Roelen B.A. Porcine oocytes are most vulnerable to the mycotoxin deoxynivalenol during formation of the meiotic spindle. Theriogenology 2010, 74:968-978.
31. Tiemann U., Dänicke S. Invivo and invitro effects of the mycotoxins zearalenone and deoxynivalenol on different non-reproductive and reproductive organs in female pigs: a review. Food Addit Contam 2007, 24:306-314.
32. Qian Y., Shi W.Q., Ding J.T., Sha J.H., Fan B.Q. Predictive value of the area of expanded cumulus mass on development of porcine oocytes matured and fertilized invitro. J Reprod Dev 2003, 49:167-174.
33. Medvedova M., Kolesarova A., Capcarova M., Labuda R., Sirotkin A.V., Kovacik J., et al. The effect of deoxynivalenol on the secretion activity, proliferation and apoptosis of porcine ovarian granulosa cells invitro. J Environ Sci Health B 2011, 46:213-219.
34. Baraño J.L.S., Hammond J.M. FSH increases the synthesis and stores of cholesterol in porcine granulosa cells. Mol Cell Endocrinol 1986, 44:227-236.
35. Veldhuis J.D., Gwynne J.T., Strauss J.F., Demers L.M., Klase P.A. Role of estradiol as a biological amplifier of gonadotropin action in the ovary: invitro studies using swine granulosa cells and homologous, lipoproteins. Endocrinology 1984, 114:2312-2322.
36. Huszenicza G., Fekete S., Szigeti G., Kulcsár M., Fébel H., Kellems R.O., et al. Ovarian consequences of low dose peroral Fusarium (T-2) toxin in a ewe and heifer model. Theriogenology 2000, 53:1631-1639.
37. Juhasz J., Nagy P., Reiczigel J., Kulcsar M., Szigeti G., Huszenicza G. Effect of certain mycotoxins contaminating feedstuff (zearalenone, T-2 toxin) and dexamethasone on the reproductive function of horses. Magyar Allatorvosok Lapja 2001, 123:475-482.
38. Caloni F., Ranzenigo G., Cremonesi F., Spicer L.J. Effects of a trichothecene, T-2 toxin, on proliferation and steroid production by porcine granulosa cells. Toxicon 2009, 54:337-344.
39. 1 in rats. Jordan J Biol Sci 2012, 5:183-190.
40. Cortinovis C. Invitro effects of fumonisin B1 alone and combined with deoxynivalenol or zearalenone on porcine granulosa cell proliferation and steroidogenesis. PhD thesis, Università degli Studi di Milano, Italy.
41. Petro E.M., Leroy J.L., Van Cruchten S.J., Covaci A., Jorssen E.P., Bols P.E. Endocrine disruptors and female fertility: focus on (bovine) ovarian follicular physiology. Theriogenology 2012, 78:1887-1900.
42. Christensen C.M., Mirocha C.J., Nelson G.H., Quast J.F. Effect of young swine of consumption of rations containing corn invaded by Fusarium roseum. Appl Microbiol 1972, 23:202.
43. Berger T., Esbenshade K.L., Diekman M.A., Hoagland T., Tuite J. Influence of prepubertal consumption of zearalenone on sexual development of boars. J Anim Sci 1981, 53:1559-1564.
44. Young L.G., King G.J. Prolonged feeding of low levels of zearalenone to young boars. J Anim Sci 1983, 57:313-314.
45. Ruhr L.P., Osweiler G.D., Foley C.W. Effect of the estrogenic mycotoxin zearalenone on reproductive potential in the boar. Am J Vet Res 1983, 44:483-485.
46. Sutkevičiene N., Bakutis B., Banys A., Karveliene B., Rutkauskas A., Sabeckienė J., et al. The effect of the estrogenic mycotoxin zearalenone on boar reproductive potential and the dynamic of aspartate aminotransferase and alanine aminotransferase levels in the boar blood serum. Vet Zootech 2009, 46:73-77.
47. Milano G.D., Odriozola E., Lopèz T.A. Lack of effect of a diet containing zearalenone on spermatogenesis in rams. Vet Rec 1991, 13:33-34.
48. Benzoni E., Minervini F., Giannoccaro A., Fornelli F., Vigo D., Visconti A. Influence of invitro exposure to mycotoxin zearalenone and its derivatives on swine sperm quality. Reprod Toxicol 2008, 25:461-467.
49. Tsakmakidis I.A., Lymberopoulos A.G., Alexopoulos C., Boscos C.M., Kyriakis S.C. Invitro effect of zearalenone and alpha-zearalenol on boar sperm characteristics and acrosome reaction. Reprod Domest Anim 2006, 41:394-401.
50. Tsakmakidis I.A., Lymberopoulos A.G., Vainas E., Boscos C.M., Kyriakis S.C., Alexopoulos C. Study on the invitro effect of zearalenone and alpha-zearalenol on boar sperm-zona pellucida interaction by hemizona assay application. J Appl Toxicol 2007, 27:498-505.
51. Tsakmakidis I.A., Lymberopoulos A.G., Khalifa T.A., Boscos C.M., Saratsi A., Alexopoulos C. Evaluation of zearalenone and alpha-zearalenol toxicity on boar sperm DNA integrity. J Appl Toxicol 2008, 28:681-688.
52. D'Occhio M.J., Hengstberger K.J., Johnston S.D. Biology of sperm chromatin structure and relationship to male fertility and embryonic survival. Anim Reprod Sci 2007, 101:1-17.
53. Yang J., Zhang Y., Wang Y., Cui S. Toxic effects of zearalenone and alpha-zearalenol on the regulation of steroidogenesis and testosterone production in mouse Leydig cells. Toxicol InVitro 2007, 21:558-565.
54. Minervini F., Lacalandra G.M., Filannino A., Nicassio M., Visconti A., Dell'Aquila M.E. Effects of invitro exposure to natural levels of zearalenone and its derivatives on chromatin structure stability in equine spermatozoa. Theriogenology 2010, 73:392-403.
55. Filannino A., Stout T.A., Gadella B.M., Sostaric E., Pizzi F., Colenbrander B., et al. Dose-response effects of estrogenic mycotoxins (zearalenone, alpha- and beta-zearalenol) on motility, hyperactivation and the acrosome reaction of stallion sperm. Reprod Biol Endocrinol 2011, 9:134.
56. Sprando R.L., Collins T.F., Black T.N., Olejnik N., Rorie J.I., Eppley R.M., et al. Characterization of the effect of deoxynivalenol on selected male reproductive endpoints. Food Chem Toxicol 2005, 43:623-635.
57. Medveová M., Kalafová A., Schneidgenová M., Maruniaková N., Leśniak A., Latacz A., et al. The effect of deoxynivalenol on rabbit spermatozoa motility invitro. J Microbiol Biotechnol Food Sci 2012, 2:368-377.
58. Alm K., Dahlbom M., Säynäjärvi M., Andersson M.A., Salkinoja-Salonen M.S., Andersson M.C. Impaired semen quality of AI bulls fed with moldy hay: a case report. Theriogenology 2002, 58:1497-1502.
59. Kovács M., Tornyos G., Matics Z., Kametler L., Rajli V., Bodnár Z., et al. Subsequent effect of subacute T-2 toxicosis on spermatozoa, seminal plasma and testosterone production in rabbits. Animal 2011, 5:1563-1569.
60. Ewuola E.O., Egbunike G.N. Effects of dietary fumonisin B1 on the onset of puberty, semen quality, fertility rates and testicular morphology in male rabbits. Reproduction 2010, 139:439-445.
61. Ogunlade J.T., Ewuola E.O., Gbore F.A., Bandyopadhyay R., Niezen J., Egbunike G.N. Testicular and epididymal sperm reserves of rabbits fed fumonisin contaminated diets. World Appl Sci J 2006, 1:35-38.
62. Gbore F.A., Egbunike G.N. Testicular and epididymal sperm reserves and sperm production of pubertal boars fed dietary fumonisin B(1). Anim Reprod Sci 2008, 105:392-397.
63. Gbore F.A. Reproductive organ weights and semen quality of pubertal boars fed dietary fumonisin B1. Animal 2009, 3:1133-1137.
64. Minervini F., Lacalandra G.M., Filannino A., Garbetta A., Nicassio M., Dell'aquila M.E., et al. Toxic effects induced by mycotoxin fumonisin B1 on equine spermatozoa: assessment of viability, sperm chromatin structure stability, ROS production and motility. Toxicol InVitro 2010, 24:2072-2078.
65. Noden D.M., De Lahunta A. Embryology of domestic animals: developmental mechanisms and malformations 1985, Williams and Wilkins, Baltimore.
66. Friend D.W., Trenholm H.L., Fiser P.S., Thompson B.K., Hartin K.E. Effect on dam performance and fetal development of deoxynivalenol (vomitotoxin) contaminated wheat in the diet of pregnant gilts. Can J Anim Sci 1983, 63:689-698.
67. Goyarts T., Dänicke S., Brüssow K.P., Valenta H., Ueberschär K.H., Tiemann U. On the transfer of the Fusarium toxins deoxynivalenol (DON) and zearalenone (ZON) from sows to their fetuses during days 35-70 of gestation. Toxicol Lett 2007, 171:38-49.
68. Tiemann U., Brüssow K.P., Dannenberger D., Jonas L., Pohland R., Jägerd K., et al. The effect of feeding a diet naturally contaminated with deoxynivalenol (DON) and zearalenone (ZON) on the spleen and liver of sow and fetus from day 35 to 70 of gestation. Toxicol Lett 2008, 179:113-117.
69. Tiemann U., Brüssow K.P., Dänicke S., Vanselow J. Feeding of pregnant sows with mycotoxin contaminated diets and their non-effect on foetal and maternal hepatic transcription of genes of the insulin-like growth factor system. Food Addit Contam 2008, 25:1365-1373.
70. Dänicke S., Brüssow K.P., Goyarts T., Valenta H., Ueberschär K.H., Tiemann U. On the transfer of the Fusarium toxins deoxynivalenol (DON) and zearalenone (ZON) from the sow to the full-term piglet during the last third of gestation. Food Chem Toxicol 2007, 45:1565-1574.
71. Tiemann U., Brüssow K.P., Küchenmeister U., Jonas L., Pohland R., Reischauer A., et al. Changes in the spleen and liver of pregnant sows and full-term piglets after feeding diets naturally contaminated with deoxynivalenol and zearalenone. Vet J 2008, 176:188-196.
72. Schoevers E.J., Santos R.R., Colenbrander B., Fink-Gremmelsb J., Roelen B.A.J. Transgenerational toxicity of Zearalenone in pigs. Reprod Toxicol 2012, 34:110-119.
73. Pérez-Martínez C., García-Iglesias M.J., Ferreras-Estrada M.C., Bravo-Moral A.M., Espinosa-Alvarez J., Escudero-Díez A. Effects of in-utero exposure to zeranol or diethylstilboestrol on morphological development of the fetal testis in mice. J Comp Pathol 1996, 114:407-418.
74. LaBorde J., Terry K.K., Howard P.C., Chen J.J., Collins T.F.X., Shackelford M.E., et al. Lack of embryotoxicity of fumonisin B1 in New Zealand white rabbits. Fundam Appl Toxicol 1997, 40:120-128.
75. Idahor K.O., Ewuola E.O., Gbore F.A., Ogunlade J.T., Salako O.A., Egbunike G.N. Reproductive performance of rabbits fed maize-based diets containing FB1 strain of Fusarium verticillioides (Sacc.). PAT 2008, 4:85-92.
76. Marasas W.F.O., Riley T.R., Hendricks K.A., Stevens V.L., Sadler T.W., Glineau-van Waes J., et al. Fumonisins disrupt sphingolipids metabolism, folate transport, and neural tube development in embryo culture and invivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 2004, 134:711-716.
77. Gelineau-van Waes J.B., Voss K.A., Stevens V.L., Speer M.C., Riley R.T. Maternal fumonisin exposure as a risk factor for neural tube defects. Adv Food Nutr Res 2009, 56:145-181.
78. Voss K.A., Riley R.T., Gelineau-van Waes J. Fumonisins. Reproductive and developmental toxicology 2011, 725-737. Elsevier. R.C. Gupta (Ed.).
79. Stevens V.L., Tang J. Fumonisin B1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J Biol Chem 1997, 272:18020-18025.
80. Gelineau-van Waes J.B., Starr L., Maddox J.R., Aleman F., Voss K.A., Wilberding J., et al. Maternal fumonisin exposure and risk for neural tube defects: mechanisms in an invivo mouse model. Birth Defects Res (Part A): Clin Mol Teratol 2005, 73:487-497.
81. Voss K.A., Riley R.T., Gelineau-van Waes J.B. Fetotoxicity and neural tube defects in CD1 mice exposed to the mycotoxin fumonisin B1. Mycotoxins 2007, 57(Suppl.):67-72.
82. Sadler T.W., Merrill A.H., Stevens V.L., Sullards M.C. Prevention of fumonisin B1-induced neural tube defects by folic acid. Teratology 2002, 66:169-176.
83. Voss K.A., Smith G.W., Haschek W.M. Fumonisins: toxicokinetics, mechanism of action and toxicity. Anim Feed Sci Techol 2007, 137:299-325.
84. Gutzwiller A., Gafner J.L., Stoll P. Effects of a diet containing Fusarium toxins on the fertility of gilts and on bulbourethral gland weight in barrows. Arch Anim Nutr 2009, 63:16-25.
85. Friend D.W., Trenholm H.L., Thompson B.K., Fiser P.S., Hartin K.E. Effect of feeding diets containing deoxynivalenol (vomitoxin) contaminated wheat or corn on the consumption weight gain, organ weight and sexual development of male and female pigs. Can J Anim Sci 1986, 66:765-775.
86. Horugel K., Vergara H. Influence of mycotoxins on growth and onset of puberty in growing female pigs. Praktische Tierarzt 2003, 84:611-614.
87. Rainey M.R., Tubbs R.C., Bennett L.W., Cox N.M. Prepubertal exposure to dietary zearalenone alters hypothalamo-hypophysial function but does not impair postpubertal reproductive function of gilts. J Anim Sci 1990, 68:2015-2022.
88. Green M.L., Diekman M.A., Malayer J.R., Scheidt A.B., Long G.G. Effect of prepubertal consumption of zearalenone on puberty and subsequent reproduction of gilts. J Anim Sci 1990, 68:171-178.
89. Edwards S., Cantley T.C., Day B.N. The effects of zearalenone on reproduction in swine. II. The effect on puberty attainment and postweaning rebreeding performance. Theriogenology 1987, 28:51-58.
90. Gbore F.A. Growth performance and puberty attainment in growing pigs fed dietary fumonisin B1. J Anim Physiol Anim Nutr 2009, 93:761-767.