Vet Med - Czech, 2009, 54(12):565-576 | DOI: 10.17221/156/2009-VETMED

The role of mycotoxins in pig reproduction: a review

A. Kanora1, D. Maes2
1 Huvepharma NV, Antwerp, Belgium
2 Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium

Mycotoxins are commonly present in feed for farm animals. Sows and gilts are highly susceptible to mycotoxins. This article presents a review describing the main mycotoxins encountered in pig feed which have a negative impact on sow fertility and reproduction. Consumption of feed that is contaminated with these mycotoxins may cause a variety of symptoms, depending on the type of mycotoxin, quantity and duration of exposure, as well as the health status and condition of the animal at the time of exposure. Two types of fungi are recognized, field fungi and storage fungi. Field fungi such as Fusarium spp., Aspergillus spp. and Claviceps spp. may produce toxins that lead to disturbed reproductive performance. Storage fungi occur if the humidity during storage is too high. In daily practice, the symptoms related to mycotoxicosis can occur at toxin concentrations below the detection limit. Knowledge of the effects of mycotoxins is expanding rapidly. Mycotoxins may still be present in feedstuffs despite negative analytical findings and because of the presence of hot spots in feed and or feedstuffs. Clinical symptoms can be very pronounced, making the diagnosis for the practitioner quite easy but in many cases the symptoms are vague and not at all present at herd level on a regular basis. The practitioner is in the first line of raising awareness in all parties whenever the first indication exists of a possible mycotoxicosis problem causing reproductive failure in breeding pigs. The problems can be resolved only if all parties involved in pig herd health take the necessary preventive measures and actions. The main toxins causing reproductive failure discussed in this article are aflatoxins, ergot alkaloids, trichothecenes and zearalenone.

Keywords: mycotoxins; zearalenone; T-2; ergot; aflatoxins; reproduction; storage fungi

Published: December 31, 2009  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Kanora A, Maes D. The role of mycotoxins in pig reproduction: a review. Vet Med-Czech. 2009;54(12):565-576. doi: 10.17221/156/2009-VETMED.
Download citation

References

  1. Alexopoulos C. (2001): Association of Fusarium mycotoxicosis with failure in applying an induction of parturition program with PGF2alpha and oxytocin in sows. Theriogenology, 55, 1745-1757. Go to original source... Go to PubMed...
  2. Alm H., Brussow K.-P., Torner H., Vanselow J., Tomek W., Danicke S., Tiemann U. (2006): Influence of Fusarium - toxin contaminated feed on initial quality and meiotic competence of gilts oocytes. Reproductive Toxicology, 22, 44-50. Go to original source... Go to PubMed...
  3. Andretta I., Lovatto P.A., Hauschild L., Dilkin P., Garcia G.G., Lanferdini E., Cavazini N.C., Mallmann C.A. (2008): Feeding of pre-pubertal gilts with diets containing zearalenone. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 60, 1227-1233. Go to original source...
  4. Barnikol H., Gruber S., Thalmann A., Schmidt H.L. (1982): Ergot poisoning in pigs (in German). Tieraertzliche Umschau, 5, 324-332.
  5. Berger T., Esbenshade K.L., Diekman M.A., Hoagland T., Tuite J. (1981): Influence of prepubertal consumption of zearalenone on sexual development of boars. Journal of Animal Science, 53, 1559. Go to original source... Go to PubMed...
  6. Berthiller F., Dall'Astra C., Schuhmacher R., Lemmens M., Adam G., Krska R. (2005): Masked mycotoxins: determination of deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromotagraphy-tandem mass spectrometry. Journal of Agricultural and Food Chemistry, 53, 3421-3425. Go to original source... Go to PubMed...
  7. Berthiller F., Sulyok M., Krska R., Schuhmacher R. (2007): Chromatographic methods for the simultaneous determination of mycotoxins and their conjugates in cereals. International Journal of Food Microbiology, 119, 33-37. Go to original source... Go to PubMed...
  8. Binder E.M. (2007): Managing the risk of mycotoxins in modern feed production. Animal Feed Science and Technology, 133, 149-166. Go to original source...
  9. Booth N.H., McDonald L.E. (1982): Veterinary Pharmacology and Therapeutics. 6th ed. Iowa State University Press, Iowa. 1093-1096.1096
  10. Chang K., Kurtz H.J., Mirocha C.J. (1979): Effects of the mycotoxin zearalenone on swine reproduction. American Journal of Veterinary Research, 40, 1260- 1267.
  11. Christensen C.M., Mirocha C.J., Nelson G.H., Quast J.F. (1972): Effect of young swine of consumption of rations containing corn invaded by Fusarium roseum. Applied Microbiology, 23, 202. Go to original source... Go to PubMed...
  12. Danicke S., Valenta H., Doll S., Ganter A., Flachowsky G. (2004): On the effectiveness of a detoxifying agent in preventing fusario-toxicosis in fattening pigs. Animal Feed Science and Technology, 114, 141-157. Go to original source...
  13. Danicke S., Doll S., Goyarts T., Valenta H., Ueberschar K.H., Flachowsky G. (2008): On the evaluation of the occurrence of the Fusarium-toxins deoxynivalenol (DON), zearalenone (ZON) and their metabolites in physiological substrates of the pig. Tieraerztliche Praxis Ausgabe Grosstiere Nutztiere, 36, 35-47. Go to original source...
  14. Desjardins A.E. (2006): Fusarium mycotoxins: Chemistry, Genetics and Biology. APS Press, St. Paul, Minnesota. 260 pp.
  15. Diekman M.A., Green M.L. (1992): Mycotoxins and reproduction in domestic livestock. Journal of Animal Science, 70, 1615-1627. Go to original source... Go to PubMed...
  16. Diekman M.A., Green M.L., Malayer J.R., Brandt K.E., Long G.G. (1986): Effect of zearalenone and estradiol benzoate on serum LH and FSH in ovariectomized gilts. Journal of Animal Science, 63 (Suppl. 1), 330.
  17. Edwards S., Cantley T.C., Rottinghaus G.E., Osweiler G.D., Day B.N. (1987a): The effects of zearalenone on reproduction in swine. I. The relationship between ingested zearalenone dose and anestrus in non-pregnant sexually mature gilts. Theriogenology, 28, 43-49. Go to original source... Go to PubMed...
  18. Edwards S., Cantley T.C., Day B.N. (1987b): The effects of zearalenone on reproduction in swine. II. The effect on puberty attainment and postweaning rebreeding performance. Theriogenology, 28, 51-58. Go to original source... Go to PubMed...
  19. Etienne M., Jemmali M. (1982): Effects of zearalenone (F2) on estrus activity and reproduction in gilts. Journal of Animal Science, 55, 1-10. Go to original source... Go to PubMed...
  20. Farnworth E.R., Trenholm H.L. (1983): The metabolism of the mycotoxin zearalenone and its effects on the reproductive tracts of young male and female pigs. Canadian Journal of Animal Science, 63, 967-975. Go to original source...
  21. Fink-Gremmels J., Malekinejad H. (2007): Clinical effects and biochemical mechanisms associated with exposure to the mycoestrogen zearalenone. Animal Feed Science and Technology, 137, 326-341. Go to original source...
  22. Flowers B., Cantley T., Day B.N. (1987): A comparison of effects of zearalenone and estradiol benzoate on reproductive function during the estrus cycle in gilts. Journal of Animal Science, 65, 1576-1584. Go to original source... Go to PubMed...
  23. Furtado R.M., Pearson A.M., Hogberg M.G., Miller E.R., Gray J.I., Aust S.D. (1982): Withdrawal time required for clearance of aflatoxins from pig tissues. Journal of Agriculture and Food Chemistry, 30, 101-106. Go to original source... Go to PubMed...
  24. Gajecki M. (2002): Zearalenone - undesirable substances in feed. Polish Journal of Veterinary Sciences, 5, 117-122.
  25. Gareis M., Bauer J., Thiem J., Plank G., Grabley S., Gedek B. (1990): Cleavage of zearalenone-glycoside, a "masked" mycotoxin during digestion in swine. Journal of Veterinary Medicine Series B, 37, 236-240. Go to original source... Go to PubMed...
  26. Glavits R., Sandor G.S., Vanyi A., Gajdacs G. (1983): Reproductive disorders caused by trichothecene mycotoxins in a large-scale pig herd. Acta Veterinaria Hungarica, 31, 173-180.
  27. Green M.L., Diekman M.A., Malayer J.R., Scheidt A.B., Long G.G. (1990): Effect of prepubertal consumption of zearalenone on puberty and subsequent reproduction of gilts. Journal of Animal Science, 68, 171-178. Go to original source... Go to PubMed...
  28. Hale O.M., Wilson, D.M. (1979): Performance of pigs on diets containing heated or unheated corn with or without aflatoxin. Journal of Animal Science, 48, 1394- 1400. Go to original source... Go to PubMed...
  29. Jacobson W.C., Harmeyer W.C., Jackson J.E., Armbrecht B., Wiseman H.G. (1978): Transmission of aflatoxins B1 into the tissues of growing pigs. Bulleting of Environmental Contamination and toxicology, 19, 156-161. Go to original source... Go to PubMed...
  30. Kauffold J., Rautenberg T., Hoffmann G., Beynon N., Schellenberg I., Sobiraj A. (2005a): A field study into the appropriateness of transcutaneous ultrasonography in the diagnoses of uterine disorders in reproductively failed pigs. Theriogenology, 64, 1546-1558. Go to original source... Go to PubMed...
  31. Kauffold J., Richter A., Sobiraj A. (2005b): Investigations into the appropriateness of the ultrasonographically ascertained uterine weight and the uterine echotexture for the prognosis of fertility in the female pig. Tieraerztliche Praxis Ausgabe Grosstiere Nutztiere, 33, 175-180. Go to original source...
  32. Kopinski J.S., Blaney B.J., Murray S.-A., Downing J.A. (2007): Effect of feeding sorghum ergot to sows during mid lactation on plasma prolactin and litter performance. Journal of Animal Physiology and Animal Nutrition, 92, 554-561. Go to original source... Go to PubMed...
  33. Kordic B., Pribicevic S., Muntanola-Cvetkovic M., Mikolic P., Nikolic B. (1992): Experimental study of the effects of known quantities of zearalenone on swine reproduction. Journal of Environmental Pathology, Toxicology and Oncology, 11, 211-215.
  34. Koshinsky H.A., Khachatourians, G.G. (1992): Trichothecene synergism, additivity and antagonism: the significance of the maximally quiescent ratio. Natural Toxins, 1, 38-47. Go to original source... Go to PubMed...
  35. Lawlor P.G., Lynch P.B. (2001): Mycotoxins in pig feeds - 1: Source of toxins, prevention and management of mycotoxicosis. Irish Veterinary Journal, 54, 117-120.
  36. Long G.G., Diekman M.A. (1984): Effect of purified zearalenone on early gestation in gilts. Journal of Animal Science, 59, 1662-1670. Go to original source... Go to PubMed...
  37. Long G.G., Diekman M.A. (1986): Characterization of effects of zearalenone in swine during early pregnancy. American Journal of Veterinary Research, 47,184-187.
  38. Long G.G., Diekman M., Tuite J.F., Shannon G.M., Vesonder R.F. (1982): Effect of Fusarium roseum corn culture containing zearalenone on early pregnancy in swine. American Journal of Veterinary Research, 43, 1599-1603.
  39. Long G.G., Turek J., Diekman M.A., Scheidt A.B. (1992): Effect of zearalenone on days 7 to 10 post-mating on blastocyst development and endometrial morphology in sows. Veterinary Pathology, 29, 60-67. Go to original source... Go to PubMed...
  40. Malekinejad H., Maas-Bakker R.F., Fink-Gremmels J. (2005): Bioactivation of zearalenone by porcine hepatic biotransformation. Veterinary Research, 36, 799-810. Go to original source... Go to PubMed...
  41. Malekinejad H., Schoevers E.J., Daemen I.J.J.M., Zijstra C., Colenbrander B., Fink-Gremmels J., Roelen B.A.J. (2007): Exposure of oocytes to the Fusarium toxins zearalenone and deoxynivalenol causes aneuploidy and abnormal embryo development in pigs. Biology of Reproduction, 77, 840-847. Go to original source... Go to PubMed...
  42. Meyer K., Usleber E., Martlbauer E., Bauer L. (2000): Occurence of zearalenone, alpha and beta - zearalenone in bile of breeding sows in relation to reproductive performances. Berliner und Munchener Tierartzliche Wochenschrift, 113, 374-379.
  43. Obremski K., Gajecki M., Zwierzchowski W., Zielonka L., Otrocka-Domagala I., Rotkiewicz T., Mikolajczyk A., Gajecki M., Polak M. (2003): Influence of zearalenone on the reproductive system cell proliferation in gilts. Polish Journal of Veterinary Sciences, 6, 239-245.
  44. Osweiler G.D. (2006): Occurrence of mycotoxins in grains and feeds. In: Straw B., Zimmerman J., D'Allaire S., Taylor D. (eds.): Diseases of Swine. 9th ed. Blackwell Publishing, Ames, Iowa. 915-929.
  45. Osweiler G.D., Stahr H.M., Beran G.W. (1990): Relationship of mycotoxins to swine reproductive failure. Journal of Veterinary Diagnostic Investigation, 2, 73-75. Go to original source... Go to PubMed...
  46. Palyusik M., Harrach B., Mirocha C.J., Pathre S.V. (1980): Transmission of zearalenone and zearalenol into porcine milk. Acta Veterinaria Academiae Scientiarum Hungarica, 28, 217-222.
  47. Rafai P., Tuboly S., Bata A., Tilly P., Vanyi A., Papp Z., Jakab L., Tury E. (1995): Effect of various levels of T-2 in the immune system of growing pigs. Veterinary Record, 136, 511-514. Go to original source... Go to PubMed...
  48. Rainy M.R., Tubbs R.C., Bennett L.W., Cox N.M. (1990): Prepubertal exposure to dietary zearalenone alters hypothalamohypophysial function but does not impair postpubertal reproductive function of gilts. Journal of Animal Science, 68, 2015-2022. Go to original source... Go to PubMed...
  49. Ramos A.J., Fink-Gremmels J., Hernandez E. (1996): Prevention of toxic effects of mycotoxins by means of non nutritive absorbent compounds. Journal of Food Protection, 59, 631-641. Go to original source... Go to PubMed...
  50. Ranzenigo G., Caloni F., Crernonesi F., Aad P.Y., Spicer L.J. (2008): Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells. Animal Reproduction Science, 107, 115-130. Go to original source... Go to PubMed...
  51. Ruhr L.P., Osweiler G.D., Foley C.W. (1983): Effect of the estrogenic mycotoxin zearalenone on reproductive potential in the boar. American Journal of Veterinary Research, 44, 483-485.
  52. Silvotti L., Petterino C., Bonomi A., Cabassi E. (1997): Immunotoxicological effects on piglets of feeding sows diets containing aflatoxins. Veterinary Record, 141, 469-472. Go to original source... Go to PubMed...
  53. Smith T.K., Az-Llano G. (2009): A review of the effect of feed-borne mycotoxins on pig health and reproduction. Sustainable Animal Production - the Challenges and Potential Developments for Professional Farming, 261-272. Go to original source...
  54. Smith T.K., McMillan E.G., Castillo J.B. (1997): Effect of feeding blends of fusarium mycotoxin-contaminated grains containing deoxynivalenol and fusaric acid on growth and feed consumption of immature swine. Journal of Animal Science, 75, 2184-2191. Go to original source... Go to PubMed...
  55. Stubblefield R.D., Honstead J.P., Shotwell O.L. (1991): An analytical survey of aflatoxins in tissues from swine grown in regions reporting 1988 aflatoxin-contaminated corn. Journal of the Association of Official Analytical Chemists, 74, 897-899. Go to original source...
  56. Thieu N.Q., Ogle B., Pettersson H. (2008): Screening of aflatoxins and zearalenone in feedstuffs and complete feeds for pigs in Southern Vietnam. Tropical Animal Health and Production, 40, 77-83. Go to original source... Go to PubMed...
  57. Tiemann U., Danicke S. (2007): 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, 24, 306-314. Go to original source... Go to PubMed...
  58. Tsakmakidis I.A., Lymberopoulos A.G., Vainas E., Boscos C.M., Kyriakis S.C., Alexopoulos C. (2007): Study on the in vitro effect of zearalenone and alpha-zearalenol on boar sperm-zona pellucida interaction by hemizona assay application. Journal of Applied Toxicology, 27, 498-505. Go to original source... Go to PubMed...
  59. Vanyi A., Glavits R., Gajdacs E., Sandor G., Jovacs F. (1991): Changes induced in newborn piglets by the trichothecene toxin T-2. Acta Veterinaria Hungarica, 39, 29-37.
  60. Volke A., Vogler B., Schollenberger M., Karlovsky P. (2004): Microbiological detoxification of mycotoxin desoxynivalenol. Journal of Basic Microbiology, 44, 147-156. Go to original source... Go to PubMed...
  61. Weaver G.A., Kurtz H.J., Mirocha C.J., Bates F.Y., Behrens J.C., Robinson T.S., Gipp W.F. (1978a): Mycotoxin-induced abortions in swine. Canadian Veterinary Journal, 19, 72-74.
  62. Weaver G.A., Kurtz H.J., Mirocha C.J., Bates F.Y., Behrens J.C., Robinson T.S. (1978b): Effect of T-2 toxin on porcine reproduction. Canadian Veterinary Journal, 19, 310-314.
  63. Weaver G.A., Kurtz H.J., Bates F.Y., Chi M.S., Mirocha C.J., Behrens J.C., Robison T.S. (1978c): Acute and chronic toxicity of T-2 mycotoxin in swine. Veterinary Record, 103, 531-535. Go to original source... Go to PubMed...
  64. Withacre M.D., Threlfall W.R. (1981): Effects of ergocryptine on plasma prolactin luteinizing hormone and progesterone in the periparturient sow. American Journal of Veterinary Research, 42, 1538-1541.
  65. Young L.G., King G.J. (1983): Prolonged feeding of low levels of zearalenone to young boars. Journal of Animal Science, 57 (Suppl. 1), 313-314.
  66. Young L.G., King G.J. (1986): Low concentrations of zearalenone in diets of mature gilts. Journal of Animal Science, 63, 1191-1196. Go to original source... Go to PubMed...
  67. Young L.G., Vesonder R.F., Funnell H.S., Simons I, Wilcock B. (1981): Moldy corn in diets of swine. Journal of Animal Science, 52, 1312-1318. Go to original source...
  68. Young L.G., Ping H., King G.J. (1990): Effects of feeding zearalenone to sows on rebreeding and pregnancy. Journal of Animal Science, 68, 15-20. Go to original source... Go to PubMed...

This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.