Potential of lactic acid bacteria for the reduction of fumonisin exposure in African fermented maize-based foods

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Fermented cereals

Most cereals are processed in some form or another to enhance the palatability of the grains; it is very rare that certain grains are consumed “raw” e.g. flax seed. Fermented cereal products have been enhanced by microorganisms grown directly on the cereal substrate. This production process is widely known as a “household art” passed down through many generations of families and produce an intricate part of diet in our foods (Egwim et al., 2013). The distinctiveness of a fermented food depends on the diversity of raw cereal substrates used and the different methods of preparation which produces varying and excellent/delightful sensory qualities in the finished fermented product. The acidic pH nature of fermentation enhances activity of microbial enzymes which reduces anti-nutrients and increases the bioavailability of minerals and other nutrients (Chelule et al., 2010). Fermentation also has the added advantage of lowering the pH which inhibits pathogen contamination, thereby extending the shelf life of the product. Some microorganisms, namely LAB, used in fermentation have antimicrobial activities against food poisoning bacteria e.g.
Lactobacillus lactis subsp. lactis produces nisin which prevents the growth of Clostridium and Bacillus spores (Chelule et al., 2010).
The most well-known fermented products of the world are alcohol, wine, vinegar, olives, yoghurt, bread and cheese. Certain fermented products are produced as delicacies, native to specific areas of the world such as atole (produced from maize), chica (alcoholic beverage produced from pineapple, barley steep liquor, and black maize dough), pozol (produced from fermented corn dough) and jamin-bang (bread produced from maize fermented) in the Americas. In Europe, there is elderberry wine (produced from elderberries) and boza (produced from fermented maize and wheat). Asia is known for adai (mixture of fermented lentils), miso (a traditional Japanese seasoning produced by fermenting soybeans with salt and koji) and rabdi (sweet, condensed-milk-based dish) (Tamang et al., 2016). In Africa the most common fermented cereal products are: akpan and gowé in Benin, ogi in Nigeria and mahewu in South Africa, which is discussed, below, in detail. The fermented cereal products discussed here are produced from maize, sorghum and wheat with a natural spontaneous fermentation process or inoculated with old stock to initiate fermentation. During a previous study (Dawlal et al., 2010), it was established that South  African maize cultivars are mainly contaminated by Fusarium verticillioides. This fungus  produces the mycotoxin, fumonisin, which is also found to be the most prevalent in maize (Dawlal et al., 2010).

Health effects

Consumption of contaminated crops or foods prepared from contaminated raw materials can cause critical or protracted toxicity in humans and animals. This can include immunological effects, organ-specific toxicity, cancer and in severe cases, causes death (Ahangarkani et al., 2014). Mycotoxins are able to work with one another to produce different toxic effects in humans and animals as they are able to produce additive, synergistic or antagonistic reactions due to their various arrangements, including their different mechanisms of action, toxicity, origins and synthetic pathways as well as route of exposure (Smith et al., 2016). Various mycosis can occur, from superficial skin disease (e.g. tinea) to invasive organ pathology (e.g. pulmonary aspergillosis) especially to those in patients that are immune compromised (Fung and Clark, 2004).
Fumonisin B1 (FB1) is the most copiously produced and most toxic fumonisin (Kumar et al., 2008) and is linked to areas with high incidence of this cancer in Eastern Cape formerly known as Transkei (Sydenham et al., 1990). According to Gelderblom et al. (1996), FB1 are hepatotoxic and has a carcinogenic affect in rats. The widely known effect of FB1 is leucoencephalomalacia in horses (Marasas et al., 1976) but they have also been known to cause severe mortality in broiler chickens (Javed et al., 1993), pulmonary oedema in pigs and duodenitis/proximal jejunitis in horses older than 2 years (D’Mello et al., 1999). The consumption of FB1 by pregnant women can cause birth defects in humans (Hendricks, 1999). Fumonisins interfere with sphingolipid metabolism (Merrill et al., 2001) that can result in liver disease and tumors in the liver and kidneys (Richard, 2007).

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Lactic acid bacterial interactions with mycotoxins

A further advantageous interaction of LAB is its ability to protect against cyanobacteria and fungal toxins which are considered to be tumour promoters (Oelschlaeger, 2010). Some studies have shown that the deactivation of mycotoxins is due to binding rather than metabolism (El-Nezami et al., 2002; Dalie et al., 2010). Binding between LAB and mycotoxin depends on the concentration of the toxin, cell density, viability of bacteria and pH value. Some studies have shown that non-viable LAB have the same binding capacity as viable LAB, but the stability/permanency of the binding are yet to be evaluated (Fuchs et al., 2008).
Literature surveys conducted have illustrated the fact that most lactic acid bacterial strains are used for binding mycotoxins (Dalié et al., 2010; Ahlberg et al., 2015), such as aflatoxin (Haskard et al., 2001; Salim et al., 2011); aflatoxin B1 (El-Nezami et al.,1998); ochratoxin A (OTA) (Fuchs et al., 2008), zearalenone (ZEN) and α-zearalenol (El-Nezami et al., 2002); deoxynivalenol (DON), nivalenol (NIV), ZEN, FB1 and FB2 (Niderkorn et al., 2006), AFB1 and patulin (Topcu et al., 2010), and FB1 and FB2 (Zhao et al., 2016). Studies conducted by Niderkorn et al. (2006) and Dalie et al. (2010) have illustrated that LAB bind fumonisins and that deactivation of fumonisins occurs to a certain degree with adhesion to LAB cell wall components occurring rather than covalent binding or metabolism (Niderkorn et al., 2009; Dalié et al., 2010; Zhao et al., 2016). Peptidoglycans, teichoic acids, proteins and polysaccharides are the components that make-up a Gram positive cell wall structure (Delcour et al., 1999; Chapot-Chartier and Kulakauskas, 2014). The components of the cell wall, the electrostatic charge of the cell wall and the electrostatic charge of the molecules can
all play a role in the binding interaction that occur between the two.

Chapter One Literature Review: Lactic acid bacterial interactions with fumonisins
1.1. Introduction
1.2. Cereals
1.3. Mycotoxins
1.4. Prebiotics, synbiotics and probiotics
1.5. Lactic acid bacterial interactions
1.6. Toxicological studies with regard to cell lines
1.7. Conclusion
1.8. References
Chapter Two Visualization and quantification of fumonisins bound by viable and non-viable lactic acid bacteria isolated from traditional fermented maize-based products, ogi and mahewu
2.1. Abstract
2.2. Introduction
2.3. Materials and Methods
2.4. Results
2.5. Discussion
2.6. Conclusion
2.7. References
Chapter Three Potential of lactic acid bacteria for the reduction of fumonisin exposure in African fermented maize-based foods
3.1. Abstract
3.2. Introduction
3.3. Materials and Methods
3.4. Results
3.5. Discussion
3.6. Conclusion
3.7. References
Chapter Four Lactic acid bacteria from ogi, a fermented indigenous African beverage, reduce toxicity of fumonisins (B1 and B2)
4.1. Abstract
4.2. Introduction
4.3. Materials and Methods
4.4. Results
4.5. Discussion
4.6. Conclusion
4.7. References
Chapter Five General discussion, General conclusion and Recommendations
5.1. General discussion
5.2. General conclusion
5.3. Recommendations
5.4. References

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