In general, pigs are considered highly susceptible to mycotoxin contamination, with young animals and female breeders being the most sensitive groups.
Aflatoxins (Afla) can cause death when administered at high levels, but the greatest impact comes from reduced reproductive and performance capabilities, suppressed immune function and various pathological effects on organs and tissues.1 Piglets fed aflatoxin-contaminated diets which were vaccinated with ovalbumin, showed decreased cell-mediated immunity and impaired lymphocyte activation.2 Thymus weight and histopathology, as well as viable alveolar macrophages were negatively influenced.3,4 In addition, cases of aflatoxin carry-over in swine have been reported with residues found in porcine liver and muscle tissues.5
Agalactia (due to interference with the release of prolactin), feed refusal and consequent weight gain reductions are classical signs of ergot alkaloid intoxication.28,29,30 Other frequently noted symptoms have been observed in the cardiovascular and central nervous system because of increased blood pressure, causing vasoconstriction and strong uterotonic effects, resulting in stillbirths and reduced pregnancy rates.30,31 Recent studies suggest that carry-over of ergot alkaloids in pigs is negligible, as no residues were detected in meat, back fat and blood serum in animals fed the highest experimental dose of about 12 mg ergot alkaloids per day.32
Fumonisins (FUM) exposure represents an issue in swine production. Numerous studies have confirmed the link between porcine pulmonary edema (PPE) and fumonisin intoxication.20 Severe lung edemas, liver and pancreas injuries, performance decreases and immune suppression were observed in exposed animals, even at low doses.20,21,22,23,24 Chronic exposure to fumonisin B1 (FB1), decreased the proliferation of undifferentiated porcine epithelial intestinal cells, altered the integrity of the intestinal epithelium and consequently facilitated the intrusion of pathogens into the body.25 FUM impaires vaccination response, reduces the level of several specific antibodies and the period of vaccine protection. The carry-over of FUM in sow milk and pork meat (mainly liver and kidneys), may only occur after a high level of exposure over a longer period.5,21,26 On the other hand, the recently discovered hydrolyzed form of Fumonisin B1, which is an enzymatic degraded form of Fumonisin B1, caused neither intestinal nor hepatic toxicity and did not impair the intestinal morphology of pigs.27
Hepatotoxic effects, decreased performance parameters, nephrotoxicity and necrosis are the major toxic effects caused by Ochratoxin (OTA). In addition, pigs showed a significant and linear reduction of daily gain with increasing doses of ingested OTA.14,15,16 This mycotoxin was observed to suppress cell-mediated immune response in pigs, resulting in reduced macrophage activity and weakened stimulation of lymphocytes.17 Furthermore, OTA tends to accumulate in kidneys, liver and muscle tissues, as well as in blood serum and, therefore, it represents a potential hazard in the human food chain.15
Among animal species, pigs show a high sensitivity to DON. Therefore, growth reduction (anorexia and decreased nutritional efficiency), impaired immune function (enhancement and suppression), and decreased reproductive performance (reduced litter size) are the most frequently observed effects.6 Moreover, it has been demonstrated that DON inhibits intestinal nutrient absorption and alters intestinal cell and barrier functions.7,8 The highest residues of DON were detected in bile, followed by the kidneys and serum. Residues were detected in the liver and in muscle tissue as well.9 Concerning influence on immunity, trichothecenes in general reduce lymphocyte proliferation, macrophage activity and antibody response to certain vaccinations and influenced immunoglobulin levels.10,11,12,13
Despite relatively low levels of acute toxicity, Zearalenone (ZEN) can have a significant impact on swine reproduction, as pigs are among the most sensitive species to this mycotoxin. Negative effects are due to the interaction of ZEN and its metabolites with estrogen receptors. ZEN increases the frequency of abortions and stillbirths in pregnant sows. In general, ZEN contaminated feed induces the swelling and reddening of vulva, false heats and false pregnancy.18 Studies investigating the carry-over of ZEN into meat and other edible tissues showed that there is only limited tissue deposition of this mycotoxin. Furthermore, no transfer of ZEN and its major metabolites into serum was detected after a ZEN administration of 56 ppb.19
About 80% of swine diseases are related to the mismanagement of feed quality, reproduction, housing conditions and biosecurity, with only 20% due to viral, bacterial or parasitic pathogens. Toxicological interactions between mycotoxins enhance the toxic effects even at low levels. Fusarium graminearum and Fusarium culmorum are known to produce several different fusariotoxins, including ZEN and DON, which are known to interact synergistically in swine. In addition, the analysis of DON often indicates the co-occurrence of other fusariotoxins such as other trichothecenes (T-2 toxin, nivalenol, diacetoxyscirpenol), zearalenone and fumonisins.
A summary on the synergistic and additive effects of mycotoxins in pigs is presented in the figure below.
Figure 1: Synergistic and additive effects in pigs
AFB1 – Aflatoxin B1; Fb1 – Fumonisin B1; DON – Deoxynivalenol; OTA – Ochratoxin A; ZEN – Zearalenone; FA – Fusaric acid; DAS – Diacetoxyscirpenol; CPA – Cyclopiazonic acid; MON - Moniliformin
Red line: synergistic effect
Dashed line: additive effect
AFB1 – Aflatoxin B1 | AFM1 – Aflatoxin M1 | DON – Deoxynivalenol | FUM – Fumonisins | OTA – Ochratoxin A | T-2 – T-2 Toxin | HT-2 – HT-2 Toxin | ZEN - Zearalenone | Ergots – Ergot, Alkaloids
- Dilkin P, Zorzete P, Mallmann CA, Gomes JDF, Utiyama CE, Oetting LL and Corrêa (2003) Toxicological effects of chronic low doses of aflatoxin B1 and fumonisin B1-cotnaining Fusarium moniliforme culture material in weaned piglets. Food and Chemical Toxicology 41: 1345-1353.
- Meissonnier GM, Pinton P, Laffitte J, Cossalter AM, Gong YY, Wild CP, Bertin G, Galtier P and Oswald IP (2008b) Immunotoxicity of aflatoxin B1: impairment of the cell-mediated response to vaccine antigen and modulation of cytokine expression. Toxicology and Applied Pharmacology 231: 142-149.
- Mocchegiani E, Corradi A, Santarelli L, Tibaldi A, DeAngelis E, Borghetti P, Bonomi A, Fabris N and Cabassi E (1998) Zinc, thymic endocrine activity and mitogen responsiveness (PHA) in piglets exposed to maternal aflatoxicosis B1 and G1. Veterinary Immunology and Immunopathology 62: 245-260.
- Liu BH, Yu FY, Chan MH and Yang YL (2002) The effects of mycotoxins, fumonisin B1 and aflatoxin B1 on primary swine alveolar macrophages. Toxicology and Applied Pharmacology 180: 197-204.
- Völkel I, Schröer-Merker E and Czerny C-P (2011) The carry-over of mycotoxins in products of animal origin with special regard to its implications for the European food safety legislation. Food and Nutrition Sciences 2: 852-867.
- Waché YJ, Valat C, Postollec G, Bougeard S, Burel C, Oswald IP and Fravalo P (2009) Impact of deoxynivalenol on the intestinal microflora of pigs. Int. J. Mol. Sci. 2009, 10: 1-17.
- Pinton P, Accensi F, Beauchamp E, Cossalter AM, Callu P, Grosjean F and Oswald IP (2008) Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses .Toxicol. Lett. 177: 215-222.
- Pinton P, Nougayrede JP and Del Rio JC (2009) The food contaminant deoxynivalenol, decreases intestinal barrier permeability and reduces claudin expression. Toxicol Appl Pharmacol 237: 41–48.
- Döll S, Dänicke S and Valenta H (2008) Residues of deoxynivalenol (DON) in pig tissue after feeding mash or pellet diets containing low concentrations. Molecular nutrition & food research 52: 727-34.
- Pang VF, Lambert RJ, Felsburg PJ, Beasley VR, Buck WB and  WM (1988) Experimental T-2 toxicosis in swine following inhalation exposure: clinical signs and effects on hematology, serum biochemistry, and immune response. Fundamental and Applied Toxicology 11: 100-109.
- Vandenbroucke V, Croubels S, Verbrugghe E, Boyen F, De BP, Ducatelle R, Rychlik I, Haesebrouck F and Pasmans F (2009) The mycotoxin deoxynivalenol promotes uptake of Salmonella typhimurium in porcine macrophages, associated with ERK1/2 induced cytoskeleton reorganization. Veterinary Research 40: 64-75.
- Overnes 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: 539-550.
- Goyarts T, Danicke S, Tiemann U and Rothkotter HJ (2006) Effect of the Fusarium toxin deoxynivalenol (DON) on IgA, IgM and IgG concentrations and proliferation of porcine blood lymphocytes. Toxicology In Vitro 20: 858-867.
- Quiroga MA, Risso MA and Perfumo CJ (2007) T-2 mycotoxin intoxication in piglets: a systemic pathological approach and apoptotic immunohistochemical studies. Braz. J. Vet. Pathol 2 (1): 16–22.
- Battacone G, Nudda A and Pulina G (2010) Effects of ochratoxin A on livestock production. Toxins 2010 (2): 1796-1824.pig
- Lawlor PG and Lynch PB (2001) Mycotoxins in pig feeds 2: clinical aspects. Irish Veterinary Journal: 172-176.
- Harvey RB, Elissalde MH, Kubena LF, Weaver EA, Corrier DE and Clement BA (1992) Immunotoxicity of ochratoxin A to growing gilts. American Journal of Veterinary Research 53: 1966-1970.
- Zinedine A, Soriano JM, Molto JC and Manes J (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem. Toxicol. 1-18.
- Goyarts D, Dänicke H, Valenta and Ueberschär KH (2007) Carry-over of Fusarium toxins (deoxynivalenol and zearalenone) from naturally contaminated wheat to pigs. Food Additives and Contaminants 24(4): 369- 380.
- Haschek WM, Gumprecht LA, Smith G, Tumbleson ME and Constable PD (2001) Fumonisin toxicosis in swine: an overview of porcine pulmonary edema and current perspectives. Environmental Health Perspectives 109(2): 251-257.
- Grenier B, Lucioli J, Pacheco G, Cossalter A.M, Moll W.D, Loureiro-Bracarense A.P, Schatzmayr G, Oswald I.P (2011) Individual and combined effects of subclinical doses of deoxynivalenol and fumonisins in piglets. Mol. Nutr. Food Res. 55 (5), 761 - 771
- Rotter BA, Prelusky DB and Pestka JJ (1996) Toxicology of deoxynivalenol (vomitoxin). Journal of Toxicology and Environmental Health 48: 1-34.
- Harrison LR, Colvin BM, Greene JT, Newman LE and Cole Jr. JR (1990). Pulmonary edema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J. Vet. Diagn. Invest.: 217-221.
- Voss KA, Smith GW and Haschek WM (2007) Fumonisins: toxicokinetics, mechanism of action and toxicity. Animal Feed Science and Technology 137: 299-325.
- Bouhet S and Oswald IP (2005) The effects of mycotoxins, fungal food contaminants, on the intestinal epithelial cell-derived innate immune response. Veterinary Immunology and Immunopathology 108: 199-209.
- Meyer K, Mohr K, Bauer J, Horn P and Kovács M (2003) Residue formation of fumonisin B1 in porcine tissues. Food Additives and Contaminants 20 (7): 639–647.
- Grenier B, Bracarense A.P.F.L, Schwartz H, Trumel C, Cossalter A.M, Schatzmayr G, Kolf-Clauw M, Moll W.D, Oswald I.P (2012) The low intestinal and hepatic toxicity of hydrolyzed fumonisin B1 correlates with its inability to alter the metabolism of sphingolipids. Biochemical Pharmacology 83, 1465 - 1473
- Bandyopadhyay R, Frederickson D, McLaren N, Odvody G and Ryley M (1998) Ergot: a new disease threat to sorghum in the Americas and Australia Ranajit Bandyopadhyay. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, India. Plant Disease 82(4): 356-367.
- Blaney BJ, Mckenzie RA, Walters JR, Taylor LF, Bewg WS, Ryley MJ and Maryam R (2000) Sorghum ergot (Claviceps africana) associated with agalactia and feed refusal in pigs and dairy cattle. Aust Vet J 78: 102-107.
- Kopinski JS, Blaney BJ, Murray S-A and Downing JA (2008) Effect of feeding sorghum ergot (Claviceps africana) to sows during mid-lactation on plasma prolactin and litter performance. Journal of Anim Physiology and Anim Nut 92: 554–561.
- Kopinski JS, Blaney BJ, Downing JA, Mcveigh JF and Murray S-A (2007) Feeding sorghum ergot (Claviceps africana) to sows before farrowing inhibits milk production. Aust Vet J 85:169–176.
- Mainka S, Dänicke S, Böhme H, Ueberschär KH, Polten S and Hüther L (2005) The influence of ergot-contaminated feed on growth and slaughtering performance, nutrient digestibility and carry over of ergot alkaloids in growing-finishing pigs. Archives of Animal Nutrition 59(6): 377-395.