Fumonisins
The underrated mycotoxins
in poultry, livestock and humans

Fumonisins are mycotoxins produced by Fusarium species, predominantly associated with maize. However, despite their harmful effects, they may not be receiving the necessary attention.

Deepthi B V and M Y Sreenivasa

Department of Studies in Microbiology, University of Mysore, India.
Email: sreenivasamy@gmail.com; mys@microbiology.uni-mysore.ac.in

Fumonisins are mycotoxins majorly produced by Fusarium verticillioides and Fusarium proliferatum species and are predominantly associated with maize and maize-based poultry and animal feeds (Dass et al., 2008; Sreenivasa et al., 2011; Deepa et al., 2016).

Cereal grains and their by-products, being major ingredients of feeds, represent an excellent substrate for the growth and reproduction of fungi and have serious consequences on the safety of foods and feeds.

In a mycological study carried out by our laboratory, 45.37% of feed mixtures collected all over Karnataka (India) showed contamination with fumonisin-producing Fusarium species (Figure 1).

Furthermore, the study revealed a frequency of 25% and 64.28% of Fusarium contamination in animal and poultry feeds, respectively.

Figure 1. Fusarium and other mycotoxigenic fungal species isolated from animal and poultry feed mixtures.

On the other hand, other fungal genera such as Aspergillus flavus, A. columnaris, A. candidus, A. niger, A. parasiticus, Penicillium, Cladosporium, Rhizopus, Helminthosporium, Mucor, sterile hyphae, etc. showed a frequency of 50% and 82.1% in animal and poultry feeds, respectively (Figure 2).

Figure 2. Per cent frequency of animal and poultry feeds showing contamination of Fusarium and other fungi.

Fumonisins are capable of inducing both acute and chronic toxic effects in poultry and livestock. These effects are dependent on:

  • The type of mycotoxin
  • The level and duration of exposure
  • The animal species that is exposed and the age of the animal

(D’mello et al., 1999)

Acute toxicity generally leads to rapid onset and an obvious toxic response, while chronic toxicity is characterized by a low-dose toxin exposure for a long time period, leading to cancer and other generally irreversible effects.

Chemically, fumonisins are toxic, cancer-promoting secondary metabolites that have:

  • A linear, 20-carbon long backbone
  • An amine group at carbon atom 2 (C-2)
  • Methyl groups at C-12 and C-16
  • Tricarballylic esters at C-14 and C-15

Fumonisins are divided into four groups based on structural differences: A, B, C and P (Musser and Plattner, 1997).

The most abundantly found and the most toxic fumonisin is fumonisin B1 (FB1):

Toxicity: FB1 is a Group 2B carcinogen (possibly carcinogenic to humans) (IARC, 2002). It has been associated with hepatotoxic, neurotoxic, nephrotoxic and immune-suppressing effects in animals and in humans.

Absorption: FB1 is poorly absorbed in the gastrointestinal tract and is extensively retained unmetabolized in tissues such as the liver and kidneys.

Excretion: FB1 is eliminated in bile through some enterohepatic recirculation while exerting its toxicity. The toxin may also end up in the faeces and as trace contaminants in urine.

Fumonisin B1 mode of action

The molecular aspects of FB1-induced toxicity are poorly understood and the downstream toxic cellular mechanisms of FB1 have been deduced to be complex, involving many molecular sites.

1. Studies have ascribed FB1-induced toxicity to the structural similarity between fumonisins and the sphingoid bases (sphinganine and sphingosine) of sphingolipid layer in cell membrane.

FB1 has a primary amino group at C-2 that competitively inhibits ceramide synthase, resulting in the disruption of de novo biosynthesis of ceramide and thus deregulating the sphingolipid complex formation (Merrill et al., 2001; Riley et al. 2001; Enongene et al. 2002; Riley and Voss, 2006).

This leads to the intracellular accumulation of sphingoid bases, increased phosphate adducts, and a reduced ceramide concentration resulting in growth inhibitory effects, cytotoxicity, apoptosis, cell proliferation, carcinogenicity, DNA damage (Riley et al., 2001; Voss et al., 2007), disruption of normal cell cycling (Ramljak et al., 2000), alteration of signalling by cAMP and protein kinase C (Huang et al., 1995), and oxidative stress (Poersch et al., 2014; Abdellatef and Khalil, 2016; Deepthi et al., 2017).

2. It has been also reported that FB1 inhibits other intracellular enzymes such as protein phosphatases and arginosuccinate synthetase (Jenkins et al., 2000).

3. In addition, Domijan and Abramov (2011) demonstrated that FB1 inhibits Complex I of the mitochondrial electron transport chain in the cell cultures of rat primary astrocytes and human neuroblastoma (SH-SY5Y).

This leads to a reduction in the rate of mitochondrial and cellular respiration, depolarization of mitochondrial membrane, over-production of reactive oxygen species (ROS) in mitochondria and deregulation of calcium signalling.

Toxic effects of Fumonisin B

Fumonisin B1 intoxication is evident in different domestic and laboratory animals and differences in sensitivity and clinical symptoms have been described (Figure 3).

Figure 3. Toxic effects of FB1 in poultry and livestock.

The first syndrome attributed to fumonisin B1 was ELEM, equine leukoencephalomalacia in the 1980s, characterized by fatal necrotic lesions in the cerebrum of horses (Marasas et al., 1988).

Fumonisin B1 induced cardiovascular dysfunction in horses with decreased heart rates, lower cardiac output, and right ventricular contractibility, which may be involved in the pathogenesis of the lesions in the central nervous system (Smith et al., 2002).

FB1 toxicosis in pigs was characterized by pulmonary, cardiovascular and hepatic symptoms. Affected animals become anorexic, showing signs of encephalopathy, loss of body weight and hepatic nodular hyperplasia.

The symptoms in swine have been referred to as Porcine Pulmonary Edema (PPE) and as “mystery swine disease” (Hollinger and Ekperigin, 1999).

For a long time, poultry has been considered to be less susceptible to fumonisins, probably because of the lack of strong clinical symptoms of impairment even with high contamination levels.

The clinical features of the disease include diarrhea, weight loss, increased liver weight and poor performance.

Recent studies have focused on the subclinical effects of fumonisins and reveal that the intestinal tract of the birds is very sensitive to the exposure to fumonisins.

Dombrink-Kurtzman et al., (1992, 1993) demonstrated that FB1 and FB2 produced cytotoxic effects on lymphocytes of turkey, and morphologically changed the peritoneal macrophages, and diminished their viability and phagocytic potential.

Chronic fumonisin-exposure in poultry has shown to have adverse effects on the immune system leading to increased pathogen susceptibility and lowered vaccinal response (Voss et al., 2007).

Additionally, ingestion of fumonisins affects the expression of proteins related to pro- and anti-inflammatory responses in the intestinal tract of broilers (Grenier and Applegate., 2013).

Rats and mice have been used extensively for decades as a model organism to study human mycotoxicosis, especially with regard to the carcinogenic potential of mycotoxins.

Pozzi et al., (2000) have reported apoptosis in the liver cells, by studying the effects of prolonged oral administration of fumonisin B1 and aflatoxin B1 in rats.

 Theumer et al., (2002) have detected immunobiological alterations produced by the ingestion of FB1 in a model of experimental subchronic mycotoxicosis in rats.

Cattle, sheep, and goats are known to be less sensitive to fumonisins. However, a negative impact on the production of milk/wool, reproduction and growth can be noticed when animals are exposed to FB1 for longer periods of time.

An in vitro study by Bernabucci et al. (2011) showed an increased production of malondialdehyde (MDA) in bovine peripheral blood mononuclear cells treated with 35 and 70 μg/mL of FB1.

A study by Goel et al., (1994) showed an increase in Sa:So ratios in serum, liver, kidney and muscle of catfish fed with ≥10 mg FB1/kg feed after 12 weeks of treatment.

An increase in serum enzymes, urea and creatinine were reported by Orsi et al. (2009) and Gbore et al. (2010) in rabbits administered oral doses of FB1.

Epidemiological incidences of esophageal cancer in humans due to the consumption of fumonisin-contaminated food have been reported from various parts of the globe such as South Africa, Central America, Asia (Rheeder et al., 1992; Chelule et al., 2001; Marasas et al., 2004) and among the dark population in Charleston, South Carolina (Sydenham et al., 1991).

Similar observations were also documented from China (Yoshizawa et al., 1994; Abnet et al., 2001), Italy (Franceschi et al., 1990), and Brazil (Van der Westhuizen et al., 2003).

An outbreak of FB1 -associated illness due to consumption of sorghum and maize contaminated with high levels of fumonisins was also reported from India characterized by acute onset of abdominal pain and diarrhea (Bhat and Krishnamachari, 1977).

Consumption of FB1 contaminated maize has also been associated with neural tube defects (due to reduction in the uptake of folic acid via folate receptor) in human infants of the rural population in South Africa and Northern China (Marasas et al., 2004).

 Environmental stress factors related to mycotoxin occurrence 

The critical difficulty in assessing the risk of different mycotoxins to animal and human health is the multiple factors affecting fungal colonization and production of mycotoxins in foods or feeds.

Environmental conditions (physical factors) are often conducive to rapid spoilage of feeds by fungi and production of harmful mycotoxins resulting in a significant decrease in the quality of feeds.

Abiotic factors or stress conditions determine the extent of fungal colonization and mycotoxin biosynthesis in crops, foods and feeds. They include:

  • Relative humidity
  • Temperature fluctuations (heat, cold, chilling, freezing)
  • Salinity
  • Drought
  • Nutrients
  • Light intensity
  • Ozone
  • pH
  • Anaerobic stresses

(Wang et al., 2003; Mitchell et al., 2004; Agarwal and Grover, 2006; Hirel et al., 2007; Cavanagh et al., 2008; Munns and Tester, 2008; Chinnusamy and Zhu, 2009; Marin et al., 2010b; Mittler and Blumwald, 2010; Faneli et al., 2012)

Optimum conditions for fungal growth are not necessarily optimum for toxin production.

Under natural conditions, the combination of two or more factors such as drought and salinity, relative humidity and temperature, heat and salinity, extreme temperature and high light intensity, etc., may have an impact on fungal infestation.

These environmental factors influence the fungal growth, metabolism and mycotoxin biosynthesis and are essential to understand the overall process and to prevent mycotoxin production and spoilage of food or feed.

Management of fumonisin contamination

The negative effects of consuming food or feed contaminated with mycotoxins have gained much attention in the public and scientific arena in the recent years.

This has generated a hitherto unprecedented interest towards the development of new detoxification procedures.

Good Agricultural Practices (GAP) and Good Manufacturing Practices (GMP) are possible methods to minimize mycotoxin occurrence in field conditions.

However, a wide gap still persists globally when it comes to implementing these practices.

Furthermore, mycotoxin contamination can be partially prevented by adapting proper processing methodologies and storage facilities of cereals, grains, food and feedstuffs.

Safe elimination of fumonisins from feed is of paramount importance as the poultry/livestock sector suffers from health-related issues and great economic losses due to fumonisins.

However, detoxification of toxins cannot be fully achieved as their production is modulated by environmental factors.

Most physical and chemical strategies followed to reduce mycotoxin contamination have been shown to be rather ineffective or are difficult to implement into the production process (Pearson et al., 2004). Moreover, fungal resistance to chemical treatments has now become widespread (Davidson, 2001).

The most commonly employed detoxification method in the poultry/livestock industry is the use of mycotoxin binders (sequestering agents) in feed, but they are usually aflatoxin-binders and have much less affinity towards fumonisins or other mycotoxins.

Therefore, a biological control method would be an efficient alternative for the management of fumonisins (Figure 4).

Figure 4. Mycotoxin management strategies in the poultry and livestock industries.

Many species of bacteria and fungi such as Flavobacterium aurantiacum, Corynebacterium rubrum, Candida lipolitica, Aspergillus niger, Trichoderma viride, Armillariella tabescens, Nuerospora species, Rhizopus species, Mucor species, etc., have been shown to enzymatically degrade mycotoxins (Bata and Lasztity, 1999; Ciegler et al., 1966).

Enzymes capable of degrading fumonisins have been isolated from a filamentous saprophytic fungus growing on maize and the corresponding genes have been cloned and transferred in transgenic maize (Blackwell et al., 1999).

Among the biocontrol agents, probiotic lactic acid bacteria (LAB) represent a potent and interesting application as they are widely used in fermented food products and feed to extend the shelf life of food/feed.

Moreover, lactic acid bacteria are GRAS “Generally Regarded as Safe” (USFDA, 2017) organisms having wide metabolic versatility and ability to produce a broad range of metabolic end products.

The possible mechanisms involved in the antifungal efficiency of LAB include:

The inhibition of mycotoxin production by LAB is due to microbial competition, depletion of nutrients, low pH, and the production of heat-stable low-molecular-weight secondary metabolites (Batish et al., 1997; Gourama and Bullerman, 1997; Laitila et al., 2002).

The mechanism by which LAB detoxifies mycotoxin remains to be elucidated. However, several reports suggest the binding nature of LAB to the mycotoxin moieties.

Lactobacilli also produce antifungal metabolites such as organic acids, hydrogen peroxide, proteinaceous compounds, hydroxyl fatty acids and phenolic compounds, offering valuable opportunities in food preservation as well as feed supplements or in veterinary medicine (Magnusson et al., 2003; Kecerova et al., 2004; Gerez et al., 2009; Bilkova et al., 2011; Cortes- Zavaleta et al., 2014; Deepthi et al., 2016).

Bacteriocin-like substances and other low and medium molecular weight compounds produced by Lactobacillus have also shown antifungal properties (Rouse et al., 2008; Kos et al., 2011; Al Kassaa et al., 2014).

The majority of studies on mycotoxins are aflatoxin-oriented, with less attention being paid to Fumonisin B1 contamination in food/ feed and their toxicity in humans/ animals.

Having a clear understanding of fumonisin interference with the living system followed by the development of chronic disorders is of immense value.

Furthermore, exploration of probiotic LAB as potent antifungal agents and as a tool to biodegrade fumonisins will guard food/feeds from fungal infestation.

These probiotic species also act as biopreservatives of food/feed and also have additive effects on health, performance and production.

Subsequently, this leads to increased food/feed production, as well as improved food/feed quality and trade/economy conditions for the countries.

REFERENCES

Abdellatef, A.A., Khalil, A.A., 2016. Ameliorated effects of Lactobacillus delbrueckii subsp lactis DSM 20076 and Pediococcus acidilactici NNRL B-5627 on Fumonisin B1-induced Hepatotoxicity and Nephrotoxicity in rats. Asian J. Pharm. Sci. 11, 326–336.

Abnet, C.C., Borkowf, C.B., Qiao, Y-L., Albert, P.S., Wang, E., Merrill, Jr A.H., Mark, S.D., Dong, Z-W., Taylor, P.R., Dawsey, S.M., 2001. Sphingolipids as biomarkers of fumonisin exposure and risk of esophageal squamous cell carcinoma in China. Cancer Causes & Control. 12(9), 821-828.

Agarwal, S., Grover, A., 2006. Molecular biology, biotechnology and genomics of flooding-associated low O2 stress response in plants. Crit. Rev. Plant Sci. 25, 1-21.

AlKassaa, I., Hamze, M., Hober, D., Chihib, N.E., Drider, D., 2014. Identification of vaginal lactobacilli with potential probiotic properties isolated from women in North Lebanon. Microb. Ecol. 67, 722–734.

Bata, A., Lasztity, R., 1999. Detoxification of mycotoxin contaminated food and feed by microorganisms. Trends Food Sci. Tech. 10, 223–228.

Batish,V.K., Roy,U., Lal,R., Grower, S., 1997. Antifungal attributes oflacticacidbacteria-areview. Crit. Rev. Biotechnol. 17, 209–225.

Bernabucci, U., Colavecchia, L., Danjeli, P.P., Basirico, L., Lacetera, N., Nardone, A., Ronchi, B., 2011. Aflatoxin B1 and fumonisin B1 affect the oxidative status of bovine peripheral blood mononuclear cells. Toxicologu in Vitro. 25(3), 684-691.

Bhat, R.V, Krishnamachari, K.A.V.R., 1977. Follow-up study of aflatoxic hepatitis in parts of western India. Indian J. Med. Res. 66, 55–58.

Bilkova, A., Sepova, H.K., Bukovsky, M., Bezakova, L., 2011. Antibacterial potential of lactobacilli isolated from a lamb. Vet. Med. 56, 319–324.

Blackwell, B.A., Gilliam, J.T., Savard, M.E., David Miller, J., Duvick, J.P., 1999. Oxidative deamination of hydrolyzed fumonisin B1 (AP1) by cultures of Exophiala spinifera. Nat Toxins. 7, 31–38.

Cavanagh, C., Morell, M., Mackey, I., Powell, W., 2008. Frpm mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr. Opin. Plant Biol. 11, 215-221.

Chelule, P.K., Ggaleni, N., Dutton, M.F., Chuturgoon, A.A., 2001. Exposure of rural and urban populations in Kwazulu Natal, South Africa, to fumonisin B1 in maize. Environ. Health Perspect. 109(3), 253-256.

Chinnusamy, V., Zhu, J.K., 2009. Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12, 133-139.

Ciegler, A., Lillehoj, E., Peterson, R., Hall, H., 1966. Microbial detoxification of aflatoxin. J. Appl. Microbiol. 14(6), 934–939.

Cortés-Zavaleta, O., López-Malo, A., Hernández-Mendoza, A., García, H.S., 2014. Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int. J. Food Microbiol. 173, 30–35.

Dass, R.S., Sreenivasa, M.Y., Janardhana, G.R., (2007) High incidence of Fusarium verticillioides in animal and poultry feed mixtures produced in karnataka, India. Plant Pathol. J. 6, 174-178.

Davidson, P.M., 2001. Chemical preservatives and natural antimicrobial compounds. In: Doyle MP, Beuchat LR, Montville TJ, editors. Food Microbiology – Fundamentals and Frontiers. 2nd Ed. American Society for Microbiology, Washington, DC. p.593-627.

Deepa, N., Nagaraja, H., Sreenivasa, M.Y., 2016. Prevalence of fumonisin producing Fusarium verticillioides associated with cereals grown in Karnataka (India). Food Science and Human Wellness. 5(3), 156-162.

Deepthi, B.V., Poornachandra Rao, K., Chennappa, G., Naik, M.K., Chandrashekara, K.T., Sreenivasa, M.Y., 2016. Antifungal attributes of Lactobacillus plantarum MYS6 against Fumonisin producing Fusarium proliferatum associated with poultry feeds. PLoS ONE. 11(6), e0155122.

Deepthi, B.V., Rakesh Somashekaraiah, Poornachandra Rao, K., Deepa, N., Dharanesha, N.K., Girish, K.S., Sreenivasa, M.Y., 2017. Lactobacillus plantarum MYS6 ameliorates fumonisinB1-induced hepatorenal damage in broilers. Front Microbiol. 8:2317.

D’mello, J., Placinta, C., Macdonald, A., 1999. Fusarium mycotoxins: A review of global implications for animal health, welfare and productivity. Anim. Feed Sci. Technol. 80, 183-205.

Dombrink-Kurtzman, M.A., Bennett, G.A., Richard, J.L., 1992. Avian lymphocytes as in vitro models to predict fumonisin cytotoxicity. FASEB J. 6, A2007.

Dombrink-Kurtzman, M.A., Javed, T., Bennett, G.A., Richard, J.L., Marie Cote, L., Buck, W.B., 1993. Lymphocyte cytoxicity and erythrocytic abnormalities induced in broiler chicks by fumonisins B 1 and B1 and moniliformin from Fusarium proliferatum. Mycpahologia. 124, 47-54.

Domijan, A.M., Abramov, A.Y., 2011. Fumonisin B1 inhibits mitochondrial respiration and deregulates calcium homeostasis – Implication to mechanism of cell toxicity. Int. J. Biochem. Cell Biol. 43, 897–904.

Enongene, E.N., Sharma, R.P., Bhandari, N., Miller, J.D., Meredith, F.I., Voss, K.A., Riley, R.T., 2002. Persistence and reversibility of the elevation in free sphingoid bases induced by fumonisin inhibition of ceramide synthase. Toxicol. Sci. 67, 173-181.

Faneli, F., Schmidt-Heydt, M., Haidukowski, M., Geisen, R., Logrieco, A., Mule, G., 2012. Influence of light on growth, fumonisin biosynthesis and FUM1 gene expression by Fusarium proliferatum. Int. J. Food Microbiol. 153, 148-153.

Franceschi, S., Bidoli, E., Baron, A.E., La Vecchia, C., 1990. Maize and risk of cancer of the oral cavity, pharynx and oesophagus in north-eastern Italy. J. Natl. Cancer. Inst. 82, 1407-1411.

Gbore, F.A., Akele, O., 2010. Growth performance, haematology and serum biochemistry of female rabbits (Oryctolagus cuniculus) fed dietary fumonisin. Veterinarski Arhiv. 80(3), 431-443.

Gerez, C.L., Torino, M.I., Rollan, G., Valdez, G.F., 2009. Prevention of bread mould spoilage by using lactic acid bacteria with antifungal properties. Food Control. 20, 144-148.

Goel, S., Lenz, S.D., Lumlertdacha, S., Lovell, R.T., Shelby, R.A., Li, M., Riley, R.T., Kemppainen, B.W., 1994. Sphingolipid levels in catfish consuming Fusarium moniliforme corn culture material containing fumonisins. Aquatic Toxicol. 30, 285-294.

Gourama, H., Bullerman, L.B., 1997. Anti-aflatoxigenic activity of Lactobacillus casei pseudoplantarum. Int. J. Food Microbiol. 34, 131-143.

Grenier, B., Applegate, T., 2013. Modulation of intestinal functions following mycotoxin ingestion: Meta-analysis of published experiments in animals. Toxins.5, 396–430.

Hirel, B., Le Gouis, J., Ney, B., Gallais, A., 2007. The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 58, 2369-2387.

Hollinger, K., Ekperigin, H,E. 1999 Mycotoxicosis in food producing animals. Vet. Clin. N. Am. Food A. 15, 133–165.

Huang, C., Dickman, M., Henderson, G., Jones, C., 1995. Repression of protein kinase C and stimulation of cyclic AMP response elements by fumonisin, a fungal encoded toxin which is a carcinogen. Cancer Res. 55, 1655-1659.

Jenkins, G.R., Tolleson W.H., Newkirk, D.K., Robert, D.W., Rowland, K.L., Seheki, T., Koyabashi, K., Howard, P.C., Melchior, W.B. 2000 Identification of fumonisin B1 as an inhibitor of argininosuccinate synthetase using fumonisin affinity chromatography and in vitro kinetic studies. J. Biochem. Mol. Toxicol. 14, 320–328.

Kecerová, K., Pristaš, P., Javorský, P., 2004. Bacteriocin production and sensitivity. Folia Microbiol. 49, 172–174. doi: 10.1007/BF02931395

Kos, B., Beganovi´C.J., Jurasic, L., Svadumovic, M., Lebos Pavunc, A., Uroic, K., Suskovic, J., 2011. Coculture-inducible bacteriocin biosynthesis of different probiotic strains by dairy starter culture Lactococcus lactis. Mljekarstvo. 61, 273–282.

Laitila, A., Alakomi, H.L., Raaska, L., Mattila-Sandholm, T., Haikara, A., 2002. Antifungal activities of two Lactobacillus plantarum strains against Fusarium moulds in vitro and in malting of barley. J. Appl. Microbiol. 93, 566-576.

Magnusson, J., Ström, K., Roos, S., Sjörgen, J., Schnürer, J., 2003. Broad and complex antifungal activity among environmental isolates of lactic acid bacteria. FEMS Microbiol. Lett. 219, 129-135.

Marasas, W.F.O., Kellerman, T.S., Gelderblom, W.C. A., Coetzer, J.A.W., Thiel, P.G., van der Lugt, J.J., 1988. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onder. J. Vet. Res. 55, 197-203.

Marasas, W.F., Riley, R.T., Hendricks, K.A., Stevens, V.L., Sadler, T.W., Waes, J.G., Missmer, S.A., Cabrera, J., Torres, O., Gelderblom, W.C., Allegood, Jl, Martinez, C., Maddox, J., Miller, J.D., Starr, L., Sullards, M.C., Roman, A.V., Voss, K.A., Wang, E., Merrill, A.H. Jr., 2004. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: A potential risk factor for human neural tube defects among populations consuming fumonisin contaminated maize. J. Nutr. 134, 711-716

Marin, P., Magan, N., Vazquez, C., Gonzab.ez-Jaen, M.Y., 2010b. Differential effect of environmental conditions on growth and regulation of the fumonisin biosynthetic gene FUM1 in the maize pathogens and fumonisin-producers Fusarium verticillioides and Fusarium proliferatum. FEMS Microbiology Ecology. 73, 303-311.

Merrill, A.H., Jr, Sullards, M.C., Wang, E., Voss, K.A., Riley, R.T. 2001. Sphingolipid metabolism: Roles in signal transduction and disruption by fumonisins. Environ. Health Perspect. 109(Suppl. 2), 283–289.

Mitchell, D., Parra, R., Aldred, D., Magan, N., 2004. Water and temperature relations of growth and ochratoxin A production by Aspergillus carbonarius strains from grapes in Europe and Israel. J. Appl. Microbiol. 97, 439-445.

Mittler, R., Blumwald, E., 2010. Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Pathol. 61, 443-462.

Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681.

Musser S M, Plattner R D. 1997. Fumonisin composition in cultures of Fusarium moniliforme, Fusarium proliferatum, and Fusarium nygami. J. Agric. Food Chem. 45(4), 1169-1173.

Orsi, R.B., Dilkin, P., Xavier, J.G., Aquino, S., Rocha, L.O., Correa, B., 2009. Acute toxicity of a single gavage dose of fumonisin B1 in rabbits. Chemico-Biological interactions. 179, 351-355.

Pearson, T., Wicklow, D., Pasikatan, M., 2004. Reduction of aflatoxin and fumonisin contamination in yellow corn by high-speed dual-wavelength sorting. Cereal Chem. 81, 490–498.

Poersch, A.B., Trombetta, F., Braga, A.C.M., Boeira, S.P., Oliveira, M.S., Dilkin, P., Mallmann, C.A., Fighera, M.R., Royes, L.F.F., Oliveira, M.S., Furian, A.F., 2014. Involvement of oxidative stress in subacute toxicity induced by fumonisin B1 in broiler chicks. Vet. Microbiol. 1988, 6–11.

Pozzi, C.R., Correa, B., Xavier, J.g., Direito, G.M., Orsi, R.B., Matarazzo, S.V., 2000. Effects of prolonged oral administration of fumonisin B1 and aflatoxin B1 in rats. Mycopathologia. 151, 21-27.

Ramljak, D., Calvert, R.J., Wiesenfeld, P.W., Diwan, B.A., Catipovic, B., Marasas, W.F.O., Victor, T.C., Anderson, L.M., Gelderblom, W.C.A., 2000. A potential mechanism for fumonisin B1-mediated hepatocarconigenesis: cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3β activity. Carcinogenesis. 21(8), 1537-1546.

Rheeder, J.P., Marasas, W.F.O., Thiel, P.G., Sydenham, E.W., Shephard, G.S., van Schalkwyk, D.J., 1992. Fusarium moniliforme and fumonisins in corn in relation to human esophageal cancer in Transkei. Phytopathol. 82, 353-357.

Riley, R.T., Enongene, E., Voss, K.A., Norred, W.P., Meredith, F.I., Sharma, R.P., Spitsbergen, J., Williams, D.E., Carlson, D.B., Merrill, A.H. Jr., 2001. Sphingolipid perturbations as mechanism for fumonisin carcinogenesis. Environ. Health Perspect. 109, 301-308.

Riley, R.T., Voss, K.A., 2006. Differential sensitivity of rat kidney and liver to fumonisin toxicity:Organ-specific differences in toxin accumulation and sphingoid base metabolism. Toxicol. Sci. 92, 335-345.

Rouse, S., Harnett, D., Vaughan, A., van Sinderen, D., 2008. Lactic acid bacteria with potential to eliminate fungal spoilage in foods. J. Appl. Microbiol. 104, 915-923.

Smith, G.W., Constable, P.D., Foreman, J.H., Eppley, R.M., Waggoner, A.L., Tumbleson, M.E., Waschek, W.M., 2002. Cardiovascular changes associated with intravenous administration of fumonisin B1 in horses. Am. J. Vet. Res. 63(4), 538-545.

M.Y. Sreenivasa, Regina Sharmila Dass, A. P. Charith Raj and G. R. Janardhana. 2011. Mycological evaluation of Maize grains produced in Karnataka (India) for the post harvest fungal contamination. World Applied Sciences Journal, 13(4), 688 – 692.

Sydenham, E.W., Shephard, G.S., Thiel, P.G., Marasas, W.F.O., Stockenstrom, S., 1991. Fumonisin contamination of commercial corn based human foodstuffs. J. Agric. Food Chem. 39, 2014-2018.

Tabata, S., Kamimura, H., Ibe, A., Hashimoto, H., Tamura, Y. 1994. Degradation of aflatoxins by food additives. J. Food Prot. 57, 42–47.

Tardieu, D., Bailly, J.D., Benard, G., Tran, T.S., Guerre, P., 2004. Toxicity of maize containing known levels of fumonisin B1 during force-feeding of ducks. Poult. Sci. 83, 1287–1293.

Tardieu, D., Bailley, J.-D., Skiba, F., Metayer, J.-P., Grosjean, F., Guerre, P., 2007. Chronic toxicity of fumonisins in turkeys. Poult. Sci. 86,
1887-1893.

Taubel, M., 2005. Isolierung und Charakterisierung von Mikroorganismen zur biologischen Inaktivierung von Fumonisinen. Doctoral Thesis. University of Natural Resources and Applied Life Sciences. Vienna, Austria. The International Agency for Research on Cancer (IARC). Monographs on the evaluation of carcinogenic risks to humans: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. 2002; 82.

Theumer, M.G., Lopez, A.G., Masih, D.T., Chulze, S.N., Rubinstein, H.R., 2002. Immunobiological effects of fumonisin B1 in experimental subchronic mycotoxicosis in rats. Clin. Diagn. Lab Immunol. 9(1), 149-155. U.S. Food and Drug Administration, 2017. GRAS Notices. http://www.accessdata.fda. gov/scripts/fdcc/?set=GRASNotices (Accessed 08.02. 17).

Van der Westhuizrn, L., Shephard, G.S., Scussel, V.M., Costa, L.L.F., Vismer, H.F., Rheeder, J.P., Marasas, W.F.O., 2003. Fumonisin contamination and Fusarium incidence in corn from Santa Catarina, Brazil. J. Agric. Food Chem. 51(18), 5574-5578.

Voss, K.A., Smith, G.W., Haschek, W.M., 2007. Fumonisins: Toxicokinetics, mechanism of action and toxicity. Anim. Feed Sci. Technol. 137, 299–325.Waalwijk, C., van der Lee, T., de Vries, I., Hesselink, T., Arts, J., Kema, G.H.J., 2004. Synteny in toxigenic Fusarium species: the fumonisin gene cluster and the mating type region as examples. Eur. J. Plant Pathol. 110, 533-544.

Wang, W., Vinocur, B., Altman, A., 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 218, 1-14.

Yoshizawa, T., Yamashita, A., Luo, Y., 1994. Fumonisin occurrence in corn from highand low-risk areas for human esophageal cancer in China. Appl. Environ. Microbiol. 60, 1626-1629.



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