In vivo and in vitro effects of the mycotoxins zearalenone and deoxynivalenol on different non-reproductive and reproductive organs in female pigs: A review

Food Additives and Contaminants

Volumn 24, Issue 3, 2007, Pages 306-314

  Tiemann, U ^a   Danicke S ^b  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

Author keywords

Deoxynivalenol; Female pig; Fusar UM toxins; Reproductive and non reproductive organs; Zearalenone

Indexed keywords

COLLAGEN; ESTROGEN; GLYCOGEN; HEMOSIDERIN; MYCOTOXIN; VOMITOXIN; ZEARALENONE;

ANIMAL FOOD; CELLULAR IMMUNITY; EMBRYO DEVELOPMENT; FEMALE; FOOD CONTAMINATION; FOOD INTAKE; FUSARIUM; HISTOPATHOLOGY; HORMONE ACTION; HUMORAL IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; LIVER DYSFUNCTION; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REPRODUCTIVE TOXICITY; REVIEW; SPLEEN DISEASE; STEROIDOGENESIS; SWINE; UTERUS DISEASE; WHEAT;

ANIMAL FEED; ANIMALS; FEMALE; FOOD CONTAMINATION; GENITALIA, FEMALE; LIVER; MYCOTOXINS; SPLEEN; SWINE; TRICHOTHECENES; UTERUS; ZEARALENONE;

FUSARIUM; SUIDAE; TRITICUM AESTIVUM;

EID: 33847110271     PISSN: 0265203X     EISSN: 14645122     Source Type: Journal    
DOI: 10.1080/02652030601053626     Document Type: Review

References (87)

1. Abouzied, MM, Azcona, JI, Braselton, WE and Pestka, JJ (1991) Immunochemical assessment of mycotoxins in 1989 grain foods: Evidence for deoxynivalenol vomitoxin contamination. Applied Environmental Microbiology, 57, pp. 672-677.
2. Alm, H., Brüssow, K-P, Torner, H., Vanselow, J., Tomek, W., Dänicke, S. and Tiemann, U. (2006) Influence of Fusarium-toxin contaminated feed on initial quality and meiotic competence of gilt oocytes. Reproductive Toxicology, 22, pp. 44-50.
3. Alm, H., Greizing, T., Brüssow, K-P, Torner, H. and Tiemann, U. (2002) The influence of the mycotoxins deoxynivalenol and zearalenol on the in vitro maturation of pig oocytes and in vitro culture of pig zygotes. Toxicology In Vitro, 16, pp. 643-648.
4. Bergsjø, B., Langseth, W., Nafstad, I., Jansen, JH and Larsen, HJS (1993) The effects of naturally deoxynivalenol-contaminated oats on the clinical condition, blood parameters, performance and carcass composition of growing pigs. Veterinary Research Communications, 17, pp. 283-294.
5. Bergsjø, B., Marte, T. and Nafstad, I. (1992) Effect of diets with graded levels of deoxynivalenol on performance in growing pigs. Journal of Veterinary Medicine, 39, pp. 752-758.
6. Biehl, ML, Prelusky, DB, Koritz, GD, Hartin, KE, Buck, WB and Trenholm, HL (1993) Biliary excretion and enterohepatic cycling of zearalenone in immature pigs. Toxicology and Applied Pharmacology, 121, pp. 152-159.
7. Bondy, GS and Pestka, JJ (2000) Immunomodulation by fungal toxins. Journal of Toxicology and Environmental Health, Part B: Critical Reviews, 3, pp. 109-143.
8. Bunner, DL and Morris, ER (1988) Alteration of multiple cell membrane functions in L-6 myoblasts by T-2 toxin: An important mechanism of action. Toxicology and Applied Pharmacology, 92, pp. 113-121.
9. Chang, K., Kurtz, HJ and Mirocha, CJ (1979) Effects of the mycotoxin zearalenone on swine reproduction. American Journal of Veterinary Research, 40, pp. 1260-1267.
10. Chelkowski, J. (1998) Distribution of Fusarium species and their mycotoxins in cereal grains. Mycotoxins in agriculture and food safety, pp. 45-66. Marcel Dekker, New York, NY
11. Dacasto, M., Rolando, P., Nachtmann, C., Ceppa, L. and Nebbia, C. (1995) Zearalenone mycotoxicosis in piglets suckling sows fed contaminated grain. Veterinary and Human Toxicology, 37, pp. 359-361.
12. Dänicke, S., Brüssow, K-P, Valenta, H., Ueberschär, K-H, Tiemann, U. and Schollenberger, M. (2005) On the effects of graded levels of Fusarium toxin-contaminated wheat in diets for gilts on feed intake, growth performance and metabolism of deoxynivalenol and zearalenone. Molecular Nutrition Food Research, 49, pp. 932-943.
13. Dänicke, S., Goyarts, T., Döll, S., Grove, N., Spolders, M. and Flachowsky, G. (2006) Effects of the Fusarium toxin deoxynivalenol on tissue protein synthesis in pigs. Toxicology Letters, 165, pp. 297-311.
14. Dänicke, S., Goyarts, T., Valenta, H., Razzazi, E. and Böhm, J. (2004) On the effects of increasing deoxynivalenol (DON) concentrations in pig feed on growth performance, utilization of nutrients and metabolism of DON. Journal of Animal and Feed Science, 13, pp. 539-556.
15. Dänicke, S., Swiech, E., Buraczewska, L. and Ueberschär, K-H (2005) Kinetics and metabolism of zearalenone in young female pigs. Journal of Animal Physiology and Animal Nutrition, 89, pp. 268-276.
16. Dänicke, S., Valenta, H., Klobasa, F., Döll, S., Ganter, M. and Flachowsky, G. (2004) Effects of graded levels of Fusarium toxin contaminated wheat in diets for fattening pigs on growth performance, nutrient digestibility, deoxynivalenol balance and clinical serum characteristics. Archives of Animal Nutrition, 58, pp. 1-17.
17. Diekman, MA and Green, ML (1992) Mycotoxins and reproduction in domestic livestock. Journal of Animal Science, 70, pp. 1615-1627.
18. Diekman, MA and Long, GG (1989) Blastocysts development on days 10 or 14 after consumption of zearalenone by sows on days 7 to 10 after breeding. American Journal of Veterinary Research, 50, pp. 1224-1227.
19. Döll, S., Dänicke, S. and Schnurrbusch, U. (2004) The effect of increasing concentrations of Fusarium toxins in piglet diets on histological parameters of the uterus and vagina. Archive of Animal Nutrition, 58, pp. 413-417.
20. Döll, S., Dänicke, S., Ueberschär, K-H, Valenta, H., Schnurrbusch, U., Ganter, M., Klobasa, F. and Flachowsky, G. (2003) Effects of graded levels of Fusarium toxin contaminated maize in diets for female weaned piglets. Archive of Animal Nutrition, 57, pp. 311-334.
21. Drochner, W., Schollenberger, M., Piepho, HP, Gotz, S., Lauber, U., Tafaj, M., Klobasa, F., Weiler, U., Claus, R. and Steffl, M. (2004) Serum IgA-promoting effects induced by feed loads containing isolated deoxynivalenol (DON) in growing piglets. Journal of Toxicology and Environmental Health, 67, pp. 1051-1067.
22. Edwards, S., Cantley, TC and Day, BN (1987) The effect of zearalenone on reproduction in pigs. II. The effect of puberty attainment and postweaning rebreeding performance. Theriogenology, 28, pp. 51-58.
23. EFSA (2004) Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to deoxynivalenol (DON) as undesirable substance in animal feed. EFSA Journal, 73, pp. 1-41.
24. EFSA (2004) Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to zearalenone as undesirable substance in animal feed. EFSA Journal, 89, pp. 1-35.
25. Ehrlich, KC and Daigle, KW (1987) Protein synthesis inhibition by 8-oxo-12,13-epoxytrichothecenes. Biochimica et Biophysica Acta, 923, pp. 206-213.
26. Ellis, TN and Beaman, BL (2004) Interferon-gamma activation of polymorphonuclear neutrophil function. Immunology, 112, pp. 2-12.
27. European Union (2006) The Commission of the European Communities Commission recommendation of 17 August 2006: On the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding. Official Journal of the European Union L 229/7
28. Farnworth, ER and Trenholm, HL (1983) The metabolism of the mycotoxin zearalenone and its effect on the reproductive tracts of young male and female pigs. Canadian Journal of Animal Science, 63, pp. 967-975.
29. Feinberg, B. and McLaughlin, CS (1989) Biochemical mechanism of action of trichothecene mycotoxins. Trichothecene mycotoxicosis: Pathophysiological effects, Vol. I, pp. 27-35. CRC Press, Boca Raton, FL
30. Fink-Gremmels, J. (1999) Mycotoxins: Their implications for human and animal health. Veterinary Quarterly, 21, pp. 115-120.
31. Fitzpatrick, DW, Picken, CA, Murphy, LC and Buhr, MM (1989) Measurement of the relative binding affinity of zearalenone, α-zearalenol and β-zearalenol for uterine and oviduct estrogen receptors in swine, rats and chickens: An indicator of estrogenic potencies. Comparative Biochemistry and Physiology, 94, pp. 691-694.
32. Gajecki, M. (2002) Zearalenone-undesirable substances in feed. Polish Journal of Veterinary Science, 2, pp. 117-122.
33. Goyarts, T., Dänicke, S. and Grove, N. (2006) Effects of the Fusarium toxin deoxynivalenol from naturally contaminated wheat on the in vivo protein synthesis of peripheral blood lymphocytes and plasma proteins in the pig. Food and Chemical Toxicology, 44, pp. 1953-1965.
34. Goyarts, T., Dänicke, S., Tiemann, U. and Rothkötter, H-J (2006) Effect of the Fusarium toxin deoxynivalenol (DON) on IgA, IgM and IgG concentrations and proliferation of porcine blood lymphocytes. Toxicology In Vitro, 20, pp. 858-867.
35. Goyarts, T., Dänicke, S., Rothkötter, HJ, Spilke, J., Tiemann, U. and Schollenberger, M. (2005) On the effects of a chronic deoxynivalenol (DON) intoxication on performance, haematological and serum parameters of pigs when diets are offered either for ad libitum consumption or fed restrictively. Journal of Veterinary Medicine A, 52, pp. 305-314.
36. Guilette Jr, LJ, Arnold, SF and McLachlan, JA (1996) Ecoestrogens and embryos - is there a scientific basis for concern?. Animal Reproduction Science, 42, pp. 13-24.
37. Haney, A., Hughes, S. and Hughes, CJ (1984) Screening of potential reproductive toxicants by use of porcine granulosa cell cultures. Toxicology, 30, pp. 227-241.
38. Hussein, SH and Brasel, JM (2001) Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology, 167, pp. 101-134.
39. Jone, C., Erickson, L., Trosko, JE and Chang, CC (1987) Effect of biological toxins on gap-junctional intercellular communication in Chinese hamster V79 cells. Cell Biology and Toxicology, 3, pp. 1-15.
40. Katzenellenbogen, BS, Katzenellenbogen, JA and Mordecai, D. (1979) Zearalenones: Characterization of the oestrogenic potency and receptor interactions of a series of fungal beta-resorcylic acid lactones. Endocrinology, 105, pp. 33-40.
41. Kordic, B., Pribicevic, S., Muntanola-Cvetkovic, M., Nicolic, P. and Nicolic, B. (1992) Experimental studies of the effects of known quantities of zearalenone on swine reproduction. Journal of Environmental Pathology, Toxicology and Oncology, 11, pp. 53-55.
42. Kuiper-Goodman, T., Scott, PM and Watanabe, H. (1987) Risk assessment of the mycotoxin zearalenone. Regulatory Toxicology and Pharmacology, 7, pp. 253-306.
43. Long, GG and Diekman, MA (1984) Effect of purified zearalenone on early gestation in gilts. Journal of Animal Science, 59, pp. 1662-1670.
44. Long, GG and Diekman, MA (1986) Characterization of effects of zearalenone in swine during early pregnancy. American Journal of Veterinary Research, 47, pp. 184-187.
45. Long, GG, Turek, J., Diekman, MA and Scheidt, AB (1992) Effect of zearaleone on days 7 to 10 post-mating on blastocyst development and endometrial morphology in sows. Veterinary Pathology, 29, pp. 60-67.
46. Lopez, TA, Odriozola, ER, Milano, GD, Sobredo, JC, Donadio, LH and Rocco, JA (1988) Hyperestrogenism in swine due to natural poisoning with zearalenone. Revista Argentina de Microbiologia, 20, pp. 119-123.
47. Malekinejad, H., Colenbrander, B. and Fink-Gremmels, J. (2006) Hydroxysteroid dehydrogenases in bovine and porcine granulosa cells convert zearalenone into its hydroxylated metabolites α-zearalenol and β-zearalenol. Veterinary Research Communications, 30, pp. 445-453.
48. Malekinejad, H., Maas-Bakker, RF and Fink-Gremmels, J. (2005) Bioactivation of zearalenone by porcine hepatic biotransformation. Veterinary Research, 36, pp. 799-810.
49. Martin, PM, Horwitz, KB, Ryan, DS and McGuire, WL (1978) Phytoestrogen interaction with estrogen receptors in human breast cancer cells. Endocrinology, 103, pp. 1860-1867.
50. Middlebrook, JL and Leatherman, DL (1989) Binding of T-2 toxin to eukaryotic cell ribosomes. Biochemical Pharmacology, 38, pp. 3103-3110.
51. Mirocha, CJ, Pathre, SV and Chrisensen, CM (1977) Zearalenone. Mycotoxins in human and animal health. Park Forest, pp. 345-364. Pathotox, IL
52. Obremski, K., Gajecki, M., Zwierzchowski, W., Zielonka, L., Otrocka-Domagala, I., Rotkiewicz, T., Mikolajczyk, A., Gajecka, M. and Polak, M. (2003) Influence of zearalenone on reproductive system cell proliferation in gilts. Polish Journal of Veterinary Science, 6, pp. 239-245.
53. Oldenburg, E., Valenta, H. and Sator, Ch (2000) Rizikoabschätzung für die Fusariumtoxinbildung und Vermeidungsstrategien bei der Futtermittelerzeugung und Fütterung, pp. 5-34. Braunschwei Landbauforschung Völkenrode, Sonderheft. SH 216
54. Olsen, M., Malmöf, K., Pettersson, H., Sandholm, K. and Kiessling, KH (1985) Plasma and urinary levels of zearalenone and alpha-zearalenol in a prepubertal gilt fed zearalenone. Acta Pharmacologica et Toxicologica, 56, pp. 239-243.
55. Olsen, M., Pettersson, H., Sandholm, K. and Kiessling, KH (1985) Quantitative liquid chromatographic method using fluorescence detection for determining zearalenone and its metabolites in blood plasma and urine. Journal of the Association of Official Analytical Chemists, 68, pp. 632-635.
56. Olsen, M., Pettersson, H., Sandholm, K., Visconti, A. and Kiessling, KH (1987) Metabolism of zearalenone by sow intestinal mucosa in vitro. Food and Chemical Toxicology, 25, pp. 681-683.
57. Olsen, M. (1989) Metabolism of zearalenone in farm animals. Fusarium: Mycotoxins, taxonomy and pathogenicity, p. p 167. Elsevier, Amsterdam
58. Øvernes, G., Matre, T., Sivertsen, T., Larsen, HJS, Langseth, W., Reitan, LJ and Jansen, JH (1997) Effects of diets with graded levels of naturally deoxynivalenol-contaminated oats on immune response in growing pigs. Journal of Veterinary Medicine A, 44, pp. 539-550.
59. Pestka, JJ and Casale, WL (1990) Naturally occurring fungal toxins. Advances in Environmental Science and Technology, 23, pp. 613-638.
60. Pestka, JJ, Zhou, HR, Moon, Y. and Chung, YJ (2004) Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: Unraveling a paradox. Toxicology Letters, 153, pp. 61-73.
61. Pestka, JJ (2003) Deoxynivalenol-induced IgA production and IgA nephropathy-aberrant mucosal immune response with systemic repercussions. Toxicology Letters, 140, pp. 287-295.
62. Price, WD, Lowell, RA and McChesney, DG (1993) Naturally occurring toxins in feedstuffs. Journal of Animal Science, 71, pp. 2556-2562.
63. Rainey, MR, Tubbs, RC, Bennett, LW and Cox, NM (1990) Prepubertal exposure to dietary zearalenone alters hypothalamo-hypophysial function but does not impair post-pubertal reproductive function of gilts. Journal of Animal Science, 6, pp. 2015-2020.
64. Rotter, BA, Prelusky, DB and Pestka, JJ (1996) Toxicology of deoxynivalenol (vomitoxin). Journal of Toxicology and Environmental Health, 48, pp. 1-34.
65. Rotter, BA, Thompson, BK, Lessard, M., Trendholm, HL and Tryphonas, H. (1994) Influence of low-level exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Fundamental and Applied Toxicology, 23, pp. 117-124.
66. Shrimanker, K., Salter, LJ and Patterson, RL (1985) Binding of steroid hormones and anabolic agents to bovine sex-hormone binding globulin. Hormone and Metabolic Research, 17, pp. 454-457.
67. Swamy, HVLN, Smith, TK, MacDonald, EJ, Boermans, HJ and Squires, EJ (2002) Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on swine performance, brain, regional neurochemistry, and serum chemistry and the efficacy of a polymeric glucomannan mycotoxin adsorbent. Journal of Animal Science, 80, pp. 3257-3267.
68. Swamy, HVLN, Smith, TK, MacDonald, EJ, Karrow, NA, Woodward, B. and Boermans, HJ (2003) Effects of feeding a blend of grains naturally contaminated with Fusarium mycotoxins on growth and immunological measurements of starter pigs, and the efficacy of a polymeric glucomannan mycotoxin adsorbent. Journal of Animal Science, 81, pp. 2792-2803.
69. Takayama, H., Shimada, N., Mikami, O. and Murata, H. (2005) Suppressive effect of deoxynivalenol, a Fusarium mycotoxin, on bovine and porcine neutrophil chemiluminescence: An in vitro study. Journal of Veterinary Medicine A, 67, pp. 531-533.
70. Thompson, WL and Wannemacher Jr, RW (1986) Structure-function relationship of 12,13-epoxytrichothecene mycotoxins in cell culture: Comparison to whole animal lethality. Toxicon, 24, pp. 985-994.
71. Tiemann, U., Brüssow, K-P, Jonas, L., Pöhland, R., Schneider, F. and Dänicke, S. (2006) Effects of diets with cereal grains contaminated by graded levels of two Fusarium toxins on selected immunological and histological parameters of spleen in gilts. Journal of Animal Science, 84, pp. 236-245.
72. Tiemann, U., Brüssow, K-P, Küchenmeister, U., Jonas, L., Kohlschein, P., Pöhland, R. and Dänicke, S. (2006) Influence of diets with cereal grains contaminated by graded levels of two Fusarium toxins on selected enzymatic and histological parameters of liver in gilts. Food and Chemical Toxicology, 44, pp. 1228-1235.
73. Tiemann, U., Tomek, W., Schneider, F. and Vanselow, J. (2003) Effects of the mycotoxins α- and β-zearalenol on regulation of progesterone synthesis in cultured granulosa cells from porcine ovaries. Reproductive Toxicology, 17, pp. 673-681.
74. Tiemann, U., Viergutz, T., Jonas, L. and Schneider, F. (2003) Influence of the mycotoxins α- and β-zearalenol and deoxynivalenol on the cell cycle of cultured porcine endometrial cells. Reproductive Toxicology, 17, pp. 209-218.
75. Tumbleson, ME and Schook, LB (1996) Advances in swine in biochemical research. In: Advances in swine in biochemical research, pp. 99-112. Plenum, New York, NY
76. Ueno, Y. (1983) General toxicology. In: Trichothecenes: Chemical, biological and toxicological aspects, pp. 135-146. Elsevier, Amsterdam
77. Weaver, GA, Kurtz, HJ, Mirocha, CJ, Bates, FY, Behrens, JC, Robison, TS and Gipp, WF (1978) Mycotoxin-induced abortions in swine. Canadian of Veterinary Journal, 19, pp. 1-74.
78. Witt, MF and Pestka, JJ (1990) Uptake of the naturally occurring 3-α-hydroxy isomer of T-2 toxin by a murine B-cell hybridoma. Food and Chemical Toxicology, 28, pp. 21-28.
79. Wollenhaupt, K., Dänicke, S., Brüssow, K-P and Tiemann, U. (2006) In vitro and in vivo effects of deoxynivalenol (DNV) on regulators of cap dependent translation control in porcine endometrium. Reproductive Toxicology, 21, pp. 60-73.
80. Wollenhaupt, K., Jonas, L., Tiemann, U. and Tomek, W. (2004) Influence of the mycotoxins α- and β-zearalenol (ZOL) on regulators of cap-dependent translation control in pig endometrial cells. Reproductive Toxicology, 19, pp. 189-199.
81. Wollenhaupt, K., Tomek, W. and Tiemann, U. (2007) Comparison of the molecular effects of the mycotoxins β-zearalenol (β-ZOL) and deoxynivalenol (DON) in porcine endometrial cells (PEC). Acta Veterinaria Hungarica, 55, pp. 123-133.
82. Wood, GE (1992) Mycotoxins in food and feeds in the United States. Journal of Animal Science, 70, pp. 3941-3949.
83. Yang, HH, Aulerich, RJ, Helferich, W., Yamini, B., Chou, KC, Miller, ER and Bursian, SJ (1995) Effects of zearalenone and/or tamoxifen on swine and mink reproduction. Journal of Applied Toxicology, 15, pp. 223-232.
84. Yoshino, N., Takizawa, M., Akiba, H., Okumura, H., Tashiro, F., Honda, M. and Ueno, Y. (1996) Transient elevation of intracellular calcium ion levels as an early event in T-2 toxin-induced apoptosis in human promyelotic cell line HL-60. Nature Toxins, 4, pp. 234-241.
85. Zhou, HR, Lau, AS and Pestka, JJ (2003) Role of double-stranded RNA-activated protein kinase R (PKR) in deoxynivalenol-induced ribotoxic stress response. Toxicology Science, 74, pp. 335-344.
86. Zöllner, P., Jodlbauer, J., Kleinova, M., Kahlbacher, H., Kuhn, T., Hochsteiner, W. and Lindner, W. (2002) Concentration levels of zearalenone and its metabolites in urine, muscle tissue, and liver samples of pigs fed with mycotoxin-contaminated oats. Journal of Agricultural and Food Chemistry, 50, pp. 2494-2501.
87. Zwierzchowski, W., Przybylowicz, M., Obremski, K., Zielonka, L., Skorska-Wyszynska, E., Gajecka, M., Polak, M., Jakimiuk, E., Jana, B. and Rybarczyk, L. (2005) Level of zearaleonene in blood serum and lesions in ovarian follicles of sexually immature gilts in the course of zearalenone microtoxicocis. Polish Journal of Veterinary Science, 8, pp. 209-218.