Mycotoxicoses in veterinary medicine: Aspergillosis and penicilliosis

Document Type: Review Article

Authors

1 Department of Pharmacology and Toxicology, Faculty of Pharmacy, Urmia University of Medical Sciences, Urmia, Iran

2 Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands

Abstract

Molds and mycotoxins are contaminants of animal feed causing spoilage and clinical intoxication. Animal exposure to mycotoxins reflects diet composition with major differences occurring between animals kept predominantly of pastures, i.e. ruminants and horses, and those consuming formulated feed like pigs and poultry. Mixed feeds are composed of several ingredients, often sourced from different continents. Subsequently, practitioners may confront endemic diseases and signs of toxin exposure related to toxins imported accidentally with contaminated feed materials from other countries and continents. Mycotoxins comprise more than 300 to 400 different chemicals causing a variety of clinical symptoms. Mycotoxin exposure causes major economic losses due to reduced performance, impaired feed conversion and fertility, and increased susceptibility to environmental stress and infectious diseases.  In acute cases, clinical symptoms following mycotoxin ingestion are often non-specific, hindering an immediate diagnosis. Furthermore, most mold species produce more than one toxin, and feed commodities are regularly contaminated with various mold species resulting in complex mixtures of toxins in formulated feeds. The effects of these different toxins may be additive, depending on the level and time of exposure, and the intensity of the clinical symptoms based on age, health, and nutritional status of the exposed animal(s). Threshold levels of toxicity are difficult to define and discrepancies between analytical data and clinical symptoms are common in daily practice. This review aims to provide an overview of Aspergillus and Penicillium toxins that are frequently found in feed commodities and discusses their effects on animal health and productivity.

Keywords


 
  1. Alshannaq A, Yu JH. Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res Public Health 2017; 14(6): E632. doi: 10.3390/ijerph14060632.
  2. Gock MA, Hocking AD, Pitt JI, et al. Influence of temperature, water activity and pH on growth of some xerophilic fungi. Int J Food Microbiol 2003; 81(1): 11-9.
  3. Blount, WP. Turkey "X" disease. Turkeys 1961, 9(2): 52,55-58,61.
  4. Santos Pereira C, Cunha SC, Fernandes JO. Prevalent mycotoxins in animal feed: Occurrence and analytical methods. Toxins 2019; 11(5): 290. doi: 10.3390/toxins 11050290.
  5. Charmley LL, Trenholm HL, Prelusky DB, et al. Economic losses and decontamination. Nat Toxins 1995; 3(4): 199-203.
  6. Miller DM, Wilson DM. Veterinary diseases related to aflatoxins. In: Eaton DL, Groopman JD (Eds). The toxicology of aflatoxins. San Diego, USA: Academic Press 1994; 347-364.
  7. Calori-Domingues MA, Bernardi CM, Nardin MS, et al. Co-occurrence and distribution of deoxynivalenol, nivalenol and zearalenone in wheat from Brazil. Food Addit Contam: Part B Surveill 2016; 9(2): 142-151.
  8. Smith JE, Solomons G, Lewis C, et al. Role of mycotoxins in human and animal nutrition and health. Nat Toxins 1995; 3(4): 187-192.
  9. Tamang JP, Watanabe K, Holzapfel WH. Review: Diversity of microorganisms in global fermented foods and beverages. Front Microbiol 2016; 7: 377. doi: 10.3389/fmicb.2016.00377.
  10. Eaton DL, Gallagher EP. Mechanisms of aflatoxin carcino-genesis. Annu Rev Pharmacol Toxicol 1994; 34: 135-172.
  11. Ramsdell HS, Eaton DL. Species susceptibility to aflatoxin B1 carcinogenesis: comparative kinetics of microsomal biotransformation. Cancer Res 1990; 50(3): 615-620.
  12. Seid A, Mama A. Aflatoxicosis and Occurrence of aflatoxin M1 (AFM1) in milk and dairy products: A Review. Austin J Vet Sci & Anim Husb. 2019; 6(1): id1054: 1-12.
  13. Arapcheska M, Jovanovska V, Jankuloski Z, et al. Impact of aflatoxins on animal and human health. Int J Innov Sci Eng Technol 2015; 2: 156-161.
  14. Marin D, Taranu I, Bunaciu RP, et al. Changes in performance, blood parameters, humoral and cellular immune responses in weanling piglets exposed to low doses of aflatoxin. J Anim Sci 2002; 80(5): 1250-1257.
  15. Bondy GS, Pestka JJ. Immunomodulation by fungal toxins. J Toxicol Environ Health B Crit Rev 2000; 3(2): 109-143.
  16. Kichou F, Walser MM. The natural occurrence of aflatoxin B1 in Moroccan poultry feeds. Vet Hum Toxicol 1993; 35(2): 105-108.
  17. Zamir‐Nasta T, Razi M, Shapour H, et al. Roles of p21, p53, cyclin D1, CDK‐4, estrogen receptor α in aflatoxin B1‐induced cytotoxicity in testicular tissue of mice. Environ Toxicol 2018; 33(4): 385-395.
  18. Motomura M, Chihaya N, Shinozawa T, et al. Cloning and characterization of the O-methyltransferase I gene (dmtA) from Aspergillus parasiticus associated with the conversions of demethylsterigmatocystin to sterig-matocystin and dihydrodemethylsterigmatocystin to dihydrosterigmatocystin in aflatoxin biosynthesis. Appl Environ Microbiol 1999; 65(11): 4987-4994.
  19. Gao W, Jiang L, Ge L, et al. Sterigmatocystin-induced oxidative DNA damage in human liver-derived cell line through lysosomal damage. Toxicol In Vitro 2015; 29(1): 1-7.
  20. Martins ML, Martins HM. Natural and in vitro coproduction of cyclopiazonic acid and aflatoxins. J Food Prot 1999; 62(3): 292-294.
  21. Steyn PS, Vleggaar R. Tremorgenic mycotoxins. Fortschr Chem Org Naturst; 1985; 48: 1-80.
  22. Ethier MF, Yamaguchi H, Madison JM. Effects of cyclopiazonic acid on cytosolic calcium in bovine airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2001; 281(1): L126-L133.
  23. Cole RJ. Etiology of turkey “X” disease in retrospect: A case for the involvement of cyclopiazonic acid. Mycotoxin Res 1986; 2(1): 3-7.
  24. Akbari P, Malekinejad H, Rahmani F, et al. Cyclopia-zonic acid attenuates the divalent cations and augments the mRNA level of iNOS in the liver and kidneys of chickens. World Mycotoxin J 2011; 5(2): 153-161.
  25. Bonyadi F, Hasanzadeh S, Malekinejad H, et al. Cyclopiazonic acid decreases sperm quality and in vitro fertilisation rate in mice. World Mycotoxin J 2018; 11(4): 599-610.
  26. Miller CD, Richard JL, Osweiler GD. Cyclopiazonic acid toxicosis in young turkeys: Clinical, physiological, and serological observations. Toxin Rev 2011; 30: 42-46.
  27. Lopez-Diaz TM, Flannigan B. Production of patulin and cytochalasin E by Aspergillus clavatus during malting of barley and wheat. Int J Food Microbiol 1997; 35(2): 129-136.
  28. Mahfoud R, Maresca M, Garmy N, et al. The mycotoxin patulin alters the barrier function of the intestinal epithelium: mechanism of action of the toxin and protective effects of glutathione. Toxicol Appl Pharmacol 2002; 181(3):209-218.
  29. Fitzpatrick LR, Wang J, Le T. Gliotoxin, an inhibitor of nuclear factor-kappa B, attenuates peptidoglycan-polysaccharide-induced colitis in rats. Inflamm Bowel Dis 2002; 8(3): 159-167.
  30. Richard JL, Dvorak TJ, Ross PF. Natural occurrence of gliotoxin in turkeys infected with Aspergillus fumigatus, Fresenius. Mycopathologia 1996; 134(3): 167-170.
  31. Jensen HE, Krogh HV, Schønheyder H. Bovine mycotic abortion-A comparative study of diagnostic methods. Zentralbl Veterinarmed B 1991; 38(1): 33-40.
  32. Eskola M, Parikka IV P, Rizzo A. Trichothecenes, ochratoxin A and zearalenone contamination and fusarium infection in Finnish cereal samples in 1998. Food Addit Contam 2001; 18(8): 707-718.
  33. Geisen R, Cantor MD, Hansen TK, et al. Characterization of Penicillium roqueforti strains used as cheese starter cultures by RAPD typing. Int J Food Microbiol 2001; 65(3): 183-191.
  34. Bailly JD, Tabuc C, Quérin A, et al. Production and stability of patulin, ochratoxin A, citrinin, and cyclopiazonic acid on dry cured ham. J Food Prot 2005; 68(7): 1516-1520.
  35. Bayman P, Baker JL, Doster MA, et al. Ochratoxin production by the Aspergillus ochraceus group and Aspergillus alliaceus. Appl Environ Microbiol 2002; 68(5): 2326-2329.
  36. O'Brien E, Heussner AH, Dietrich DR. Species-, sex-, and cell type-specific effects of ochratoxin A and B. Toxicol Sci 2001; 63(2): 256-264.
  37. Stoev SD, Vitanov S, Anguelov G, et al. Experimental mycotoxic nephropathy in pigs provoked by a diet containing ochratoxin A and penicillic acid. Vet Res Commun 2001; 25(3): 205-223.
  38. Müller G, Kielstein P, Rosner H, et al. Studies of the influence of ochratoxin A on immune and defence reactions in weaners. Mycoses 1999; 42(7‐8): 495-505.
  39. Kupski L, Freitas M, Ribeiro D, et al. Ochratoxin A activates neutrophils and kills these cells through necrosis, an effect eliminated through its conversion into ochratoxin α. Toxicology 2016; 368-369: 91-102.
  40. Hussein HS, Brasel JM. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 2001; 167(2): 101-134.
  41. Otteneder H, Majerus P. Ochratoxin A (OTA) in coffee: Nation-wide evaluation of data collected by German Food Control 1995-1999. Food Addit Contam 2001; 18(5): 431-435.
  42. Gilbert J, Brereton P, MacDonald S. Assessment of dietary exposure to ochratoxin A in the UK using a duplicate diet approach and analysis of urine and plasma samples. Food Addit Contam 2001; 18(12): 1088-1093.
  43. Peraica M, Domijan AM, Fuchs R, et al. The occurrence of ochratoxin A in blood in general population of Croatia. Toxicol Lett 1999; 110(1-2): 105-112.
  44. Braunberg RC, Barton CN, Gantt OO, et al. Interaction of citrinin and ochratoxin A. Nat Toxins 1994; 2: 124-131.
  45. Wu TS, Yang JJ, Yu FY, et al. Evaluation of nephrotoxic effects of mycotoxins, citrinin and patulin, on zebrafish (Danio rerio) embryos. Food Chem Toxicol 2012; 50(12): 4398-4404.
  46. Boysen ME, Jacobsson KG, Schnürer J. Molecular identification of species from the Penicillium roqueforti group associated with spoiled animal feed. Appl Environ Microbiol 2000; 66(4): 1523-1526.
  47. Müller HM, Amend R. Formation and disappearance of mycophenolic acid, patulin, penicillic acid and PR toxin in maize silage inoculated with Penicillium roqueforti. Arch Tierernahr 1997; 50(3): 213-225.
  48. Hochsteiner W, Schuh M, Luger K, et al. Effect of myco-toxin contaminated feed on production parameters of dairy cows. Berl Munch Tierarztl Wochenschr 2000; 113(1): 14-21.
  49. Reddy P, Guthridge K, Vassiliadis S, et al. Tremorgenic mycotoxins: Structure diversity and biological activity. Toxins 2019; 11(5): E302. doi: 10.3390/toxins11050302.
  50. Imlach WL, Finch SC, Zhang Y, et al. Mechanism of action of lolitrem B, a fungal endophyte derived toxin that inhibits BK large conductance Ca2+-activated K+ channels. Toxicon 2011; 57(5): 686-694.
  51. Knaus HG, McManus OB, Lee SH, et al. Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry 1994; 33(19): 5819-5828.
  52. McLeay LM, Smith BL, Munday-Finch SC. Tremorgenic mycotoxins paxilline, penitrem and lolitrem B, the non-tremorgenic 31-epilolitrem B and electromyographic activity of the reticulum and rumen of sheep. Res Vet Sci 1999; 66(2): 119-127.
  53. Ramos AJ, Fink-Gremmels J, Hernández E. Prevention of toxic effects of mycotoxins by means of nonnutritive adsorbent compounds. J Food Prot 1996; 59(6): 631-641.
  54. Trombete F, Freitas-Silva O, Saldanha T, et al. Ozone against mycotoxins and pesticide residues in food: Current applications and perspectives. ‎Int Food Res J 2016; 23(6): 2545-2556.
  55. Bailey RH, Kubena LF, Harvey RB, et al. Efficacy of various inorganic sorbents to reduce the toxicity of aflatoxin and T-2 toxin in broiler chickens. Poult Sci 1998; 77(11): 1623-1630.
  56. Sabater-Vilar M, Malekinejad H, Selman MH, et al. In vitro assessment of adsorbents aiming to prevent deoxynivalenol and zearalenone mycotoxicoses. Mycopathologia 2007; 163(2): 81-90.
  57. Joannis-Cassan C, Tozlovanu M, Hadjeba-Medjdoub K, et al. Binding of zearalenone, aflatoxin B1, and ochratoxin A by yeast-based products: a method for quantification of adsorption performance. J Food Prot 2011; 74 (7): 1175-1185.
  58. Megharaj M, Garthwaite I, Thiele JH. Total biodegra-dation of the oestrogenic mycotoxin zearalenone by a bacterial culture. Lett Appl Microbiol 1997;24: 329-333.
  59. Oatley JT, Rarick MD, Ji GE, et al. Binding of aflatoxin B1 to bifidobacteria in vitro. J Food Prot 2000; 63(8): 1133-1136.
  60. Azziz-Baumgartner E, Lindblade K, Gieseker K et al. Case-control study of an acute aflatoxicosis outbreak, Kenya, 2004. Environ Health Perspect 2005; 113(12):1779-1783.