Food Control 106 (2019) 106731

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Review

Food fermentation and mycotoxin detoxification: An African perspective T

∗
Janet Adeyinka Adebiyi , Eugenie Kayitesi, Oluwafemi Ayodeji Adebo, Rumbidzai Changwa,
Patrick Berka Njobeh∗∗
Department of Biotechnology and Food Technology, University of Johannesburg, P.O. Box 17011, Doornfontein, Johannesburg, South Africa

A R T I C LE I N FO A B S T R A C T

Keywords: Mycotoxins are toxigenic fungal secondary metabolites and known carcinogens that pose a significant threat to
Fermentation economies, trade, health and compromises food safety. Favourable environmental conditions on the African
Fermented foods continent encourage the proliferation of fungal species, increasing the possibility of attendant mycotoxins to be
Mycotoxins present in foods, a situation that aggravates challenges to address them. Due to the susceptibility of common
Africa
food crops to these toxins and the general inability of some conventional food processes to eliminate them, they
Food safety
Mycotoxin control
are found in derived/processed foods. Detoxification and reduction of mycotoxins in the food chain still remains
a significant topic necessitating a sustainable, affordable and effective strategy for mycotoxin control.
Fermentation of food confers desirable properties and improves food quality. This food processing technique is
also a notable inexpensive mycotoxin decontamination strategy that can be explored not only to improve the
constituents in food, but equally reduce and at best eliminate mycotoxins. In the absence of sophisticated
monitoring and prevention mechanisms in Africa, exploiting fermentation would be vital in improving nutrition
and ensuring food safety. While this processing technique generally favours mycotoxin reduction, preventing the
occurrence of these toxins in crops, effective handling and storage practices before fermentation may ensure
complete prevention of the heinous effect of these toxins on human health.

1. Introduction
In Africa, as with the rest of the world, fermented foods are known
to constitute a significant part of nutrition. On a global scale, predic-
tions indicate that the market for fermented products and ingredients
may reach up to $28.4 billion by 2022 (Sivamurati, Kesika, &
Chaiyasut, 2019). In the past decade, changes in food consumption
pattern and nutritional habits have further accelerated and increased
the consumption of fermented foods, due to their role in combating
chronic non-communicable diseases (Adebo et al., 2017a; Gille,
Schmid, Walther, & Vergeres, 2018). Fermented foods have thus been
labeled “functional foods” due to their substantiated health benefits and
as such, their consumption is increasingly encouraged (Adebiyi,
Obadina, Adebo, & Kayitesi, 2018; Makwana & Haiti, 2019).
Despite the beneficial components and health promoting attributes
of fermented foods, there have been concerns about their safety.
Contamination from raw materials/substrates used for fermentation,
unwanted toxic contaminants and foreign materials introduced during
the fermentation process, and the growth of undesirable pathogenic
microorganisms, which produce harmful metabolites, all pose a
significant threat to the safety of these foods. Significant among these
microorganisms are toxigenic fungal species including members belong
to the Aspergillus, Penicillium and Fusarium genera known to add to the
microbiota of fermented foods. These pervasive toxigenic fungal species
produce toxic secondary metabolites known as mycotoxins (Gbashi
et al., 2019; Njobeh, Dutton, & Makun, 2010).
The presence of mycotoxins in food has an adverse effect on both
human and animal health. With conducive and favourable climatic
conditions in Africa, comes increased fungal proliferation, which fur-
ther aggravates mycotoxin contamination. This is well reflected in se-
vere cases of mycotoxin contamination and exposure leading to severe
health challenges, and in severe circumstances, death of both humans
and animals occurs in different African nations as well as obvious socio-
economic impact (Gbashi et al., 2019). Not only are these mycotoxins a
problem in food safety, their presence in food also hinder metabolism
and viability of fermenting microorganisms, which negatively influ-
ences food quality (Nathanail et al., 2016).
This dire situation necessitates the need for adequate control mea-
sures for mycotoxin contamination to be put in place to safeguard the
populace. Different physical and chemical control methods have been

∗
Corresponding author.
∗∗
Corresponding author.
E-mail addresses: janetaadex@gmail.com (J.A. Adebiyi), pnjobeh@uj.ac.za (P.B. Njobeh).

https://doi.org/10.1016/j.foodcont.2019.106731
Received 4 May 2019; Received in revised form 15 June 2019; Accepted 21 June 2019
Available online 22 June 2019
0956-7135/ © 2019 Elsevier Ltd. All rights reserved.
J.A. Adebiyi, et al.
explored in the past with limited success, which is in part due to high
costs involved, safety of subsequent products, unfriendly by-products
and challenges with marketability (Adebo, Njobeh, Gbashi, Nwinyi, &
Mavumengwana, 2017b). Biological decontamination methods are
gradually becoming prominent for mycotoxin control due to high ac-
ceptance rates by consumers as compared to other decontamination
methods, thus limiting significant losses with respect to aesthetic
quality of end products (Adebo et al., 2017b; He & Zhou, 2010). Con-
sidering an array of different fermented foods in Africa and the in-
creasing reports of mycotoxin contamination in African and non-
African food crops, there is need to explore a cheap, readily available
and simple technique that would not only ensure the safety of food, but
also contribute to its sensorial, nutritional and health beneficial com-
position.
2. Mycotoxins and their control
Mycotoxins generally refer to secondary metabolites from fila-
mentous toxigenic fungi. These toxins are ubiquitous in nature and
proliferate in various food commodities as well as farming systems
(Changwa et al., 2018). The complexities of the food chain have further
contributed to mycotoxin contamination making it one of the most
daunting challenges hampering food safety, as evident in their nu-
merous deleterious health and socio-economic effects. Since the de-
tection of aflatoxins (AFs) in 1960, over 400 forms of mycotoxins have
been identified and characterized, but those considered in Africa sig-
nificant in terms of widespread occurrence, economic and health effects
they pose are the aflatoxins (AFs), fumonisins (FBs), ochratoxins (OTs),
patulin (PAT), the trichothecenes (THs) [deoxynivalenol (DON)] and
zearalenone (ZEA) (Gbashi et al., 2019). Other notable ones include
alternariol (AOH), citrinin (CIT) and ZEA derivatives [alpha-zearalenol
(α-ZEA) and beta-zearalenol (β-ZOL)] (Bryden, 2012). These natural
fungal contaminants are principally produced by various toxigenic
fungal strains of Aspergillus, Alternaria, Fusarium and Penicillium genera.
These mycotoxins occur in food crops and derived food products
and cause mycotoxicoses (diseases derived from mycotoxin exposure),
which can result in chronic or acute poisoning. The toxic effects of these
mycotoxins may however, vary according to the type of mycotoxin and
duration as well as level of exposure. These health effects are mani-
fested in various forms being implicated in causing or contributing to
hepatocellular carcinoma, oesophageal cancer, human nephropathies,
hepatitis B, liver cancers, increased mortality and morbidity, gyneco-
mastia with testicular atrophy, decreased levels of secretory im-
munoglobulin A (IgA), child undernutrition and in extreme cases,
deaths on the African continent (Gbashi et al., 2019; Kimanya,
Tiisekwa, & Mpolya, 2012; Lewis et al., 2005; Peraica, Richter, & Rašić,
2014; Shephard, 2008).
Not only do these mycotoxins cause negative health effects, they
also hamper food safety and security in Africa, thus necessitating
strategies for their prevention and reduction along the food chain.
These strategies can broadly be categorized as pre- and post-harvest
strategies as depicted in Fig. 1. The best practicable strategy for the
prevention of mycotoxin occurrence is via breeding of crops resistant to
fungal invasion and enhancing genetic composition to suppress myco-
toxin production (Halasz, Lasztity, Abonyi, & Bata, 2009). Advanced
biotechnological manipulations as observed with Aflasafe, a biocontrol
product containing a mixture of four fungal strains coated onto grains,
which mitigates against aflatoxigenic fungi that produce AFs in maize
and groundnuts (https://aflasafe.com/). The product is, in fact, cur-
rently available in few African countries (Burkina Faso, Ghana, Kenya,
Nigeria, Senegal and The Gambia), with indications of imminent
availability in other African countries. While there are general concerns
regarding genetic modification and such biocontrol measures, reports
have indicated the effective use of this product and drastic reduction of
AFs in areas it was applied. Other pre-harvest strategies include the
implementation of basic field management systems through good
2
Food Control 106 (2019) 106731
Mycotoxin Control
Pre-harvest measures Post-harvest measures
- Chemical/biological agents - Chemical control
- Physical control
- GAP - Biological control
- Ensuring maturity before - HACCP
harvest
Fig. 1. Strategies for the prevention and control mycotoxin contamination.
agricultural practices (GAP), which complements the prerequisite ha-
zard analysis and critical control point (HACCP) systems applied on the
same produce from farm to fork and the use of chemical or biological
agents as a defense line against problematic fungal species likely to
compromise quality (Adegoke & Letuma, 2013; Gashaw, 2015). Equally
important during harvest is the use of effective harvesting methods that
would prevent mechanical damage that might expose plant tissues and
ensuring that only mature crops are harvested.
Adopting these aforementioned strategies may still not completely
provide solution to the mycotoxin problem, thus requiring further post-
harvest measures to mitigate against mycotoxin exposure. Available
physical means aimed at reducing mycotoxins include grading/sorting/
segregating visibly contaminated portion from a batch, winnowing,
washing, decortication (to remove seed coat) and drying to critical
water content safe for storage of raw materials while ensuring adequate
hygiene and management of storage facilities. Implementation of pre-
ventative post-harvest HACCP approaches also aids in mycotoxin con-
trol by ensuring frontline defense against additional contamination.
Documents such as the FAO/IAEA (2001) manual details geographical
climate-based generic HACCP programs for control of mycotoxins. Such
document re-emphasizes the need to develop a product/produce-spe-
cific HACCP plan and applying the seven principles of HACCP as de-
fined by the Codex Alimentarius Commission. Additionally is a required
understanding of the vital aspects of the mycotoxin production chain.
These include a knowledge of the interactions of the mycotoxigenic
fungi with respective crops, on-farm production and effective harvest
methods for crops, development of processed foods for human con-
sumption (fermented foods in this context) as well as understanding the
marketing and trade channels including storage and delivery system of
foods to consumer (Richard, 2007). Available studies presented in the
literature in this regard have demonstrated the effective use of HACCP-
based approaches for the reduction of mycotoxins in cereals (Aldred &
Magan, 2004), peanuts (Murphy, Hendrich, Landgren, & Bryant, 2006),
kenkey (a fermented maize product) (Amoa-Awua et al., 2007), wine-
making (Martínez-Rodríguez & Carrascosa, 2009) and these toxins in
the Brazilian groundnut-based food industry (Toregeani-Mendes et al.,
2011). Such HACCP approach is effective as evident in the study of
Atter, Ofori, Anyebuno, Amoo-Gyasi, and Amoa-Awua (2015) in which
a training manual for ice-kenkey producers in Accra, Ghana was de-
veloped based on the findings of assessing the safety of the fermented
product.
Recent technological advances have equally opened the way for
strategies for mycotoxin control, which include the use of controlled
atmosphere with preservative or inhibitory action, the use of essential
oils with antioxidant activity and naturally occurring compounds under
different conditions to reduce fungal growth and mycotoxin con-
tamination in grains during storage (Gil, Ruiz, Font, & Manyes, 2016;
J.A. Adebiyi, et al. Food Control 106 (2019) 106731

Goncalves et al., 2019). Chemical techniques including the use of am- Table 1
monia and nixtamalization have also been adopted. However, appli- Some African fermented food products.
cation of such methods on a large scale or amongst small to medium Product Produce Country/Region
processors particularly within Africa remains improbable based on
costs. Furthermore, not all of these approaches necessarily meet the Animal products
Amasi Cow milk Southern Africa
desired safety and efficacy (Adebo et al., 2017b; Wu et al., 2009),
Bonome Fish Ghana
leading to the search for more suitable strategies that could be put in Ergo Milk Ethiopia
place. Leban Milk Morocco
Biological control through detoxification/degradation of myco- Mabisi Milk Zambia
toxins offers a more promising alternative of controlling mycotoxins as Nono Milk West Africa
Sethemi Milk South Africa
it entails the removal of these toxins through microbial pathways to
Wara Milk Nigeria
presumably less/non-toxic intermediates and end products (Kolosova & Cereals
Stroka, 2011; Adebo, Njobeh, Sidu, Adebiyi, & Mavumengwana, Ambga Sorghum Cameroon
2017c). Although the use of pure microbial strains has been effective Am-som Sorghum, millet or maize Nigeria
Banku Maize Ghana
for mycotoxin decontamination in vitro (Wu et al., 2009; Adebo,
Ben saalga Millet Burkina Faso
Njobeh, & Mavumengwana, 2016a, b; Adebo et al., 2017b,c; Taheur, Borde Barley, maize or wheat Ethiopia
Kouidhi, Al Quarashi, Salah-Abbes, & Chaieb, 2019), the effectiveness Bouza Wheat Egypt
of fermentation for the reduction and elimination of mycotoxins has Burukutu Sorghum or cassava Nigeria
also been demonstrated. Such additional benefits make fermentation a Busa Millet or rice Egypt
Bushera Sorghum Uganda
viable traditional food processing technique that does not only improve
Chibuku Sorghum Botswana and Zimbabwe
beneficial components, but also contributes to food safety. This is ex- Chibwantu Maize Zambia
plored in the succeeding section of this review. Degue Millet Burkina Faso
Doro Millet, sorghum Zimbabwe
3. Fermentation and mycotoxin reduction Hussuwa Sorghum Sudan
Injera Barley, maize, millet or Ethiopia, Eritrea and Sudan
sorghum
Fermentation is a process involving the utilization of microorgan- Kenkey Maize West Africa
isms for deliberate transformation of food, which occurs through me- Keribo Barley Ethiopia
tabolic activities of these microorganisms. Fermentation is an age long Kisra Sorghum Sudan
Koko Millet Ghana
food processing and preservation technique used for centuries without
Kunun-zaki Millet or sorghum Nigeria
any prior knowledge and understanding of the biochemistry/micro- Kwete Maize Uganda
biology of the process. Subsequently derived fermented foods are ubi- Mahewu Maize or sorghum South Africa and Zimbabwe
quitous, being produced from a broad range of substrates, including but Mawe Maize Benin and Ghana
not limited to cereals, animal products, roots and tubers as well as le- Merissa Sorghum Sudan
Munkoyo Maize or millet Southern Africa
gumes (Franz et al., 2014; Adebo et al., 2017a, 2018; Adebiyi et al., Ogi Maize or sorghum Ghana and Nigeria,
2018). A summary of these African fermented foods and their countries Pito Sorghum Burkina Faso, Ghana and
of origin is presented in Table 1. Nigeria
Forms of food fermentation include acetic acid, alcoholic, lactic acid Poptopoto Maize Congo
Shamsy bread Wheat Egypt
and alkali fermentation (Blandino, Al-Aseeri, Pandiella, Cantero, &
Tchapalo Maize Cote d’Ivoire
Webb, 2003). In alcoholic fermentation, yeasts are the predominant Ting Maize or sorghum Botswana and South Africa
microorganisms, a process resulting in ethanol production, while acetic Uji Maize, sorghum or millet East Africa
acids are usually produced in acetic acid fermentation through the ac- Legume/pulses and oil seeds
tions of Acetobacter species (Oliveira, Zannini, & Arendt, 2014). In le- Dawadawa Bambara groundnut or locust West and Central Africa
bean
gumes and animal products, particularly fish, alkali fermentation Iru Locust bean Nigeria
usually occurs with Bacillus species fermenting substrates to an in- Ogiri Melon or sesame seeds West Africa
creasing alkaline pH (Adebo et al., 2017b; Blandino et al., 2003). Lactic Ugba African oil bean West and Central Africa
acid fermentation is, however, the most common form of fermentation Root and Tubers
Agbelima Cassava Ghana
and it is typically carried out by lactic acid bacteria (LAB) (Gänzle,
Chikawngue Cassava Zaire
2015; Liptakova, Matejcekova, & Valik, 2017). These food fermentation Elubo Yam Nigeria
forms could either be through natural (spontaneous), back-slopping or Fufu Cassava Nigeria
controlled fermentation. Gari Cassava West Africa
The fermentation process also involves activation of enzymes, me-
tabolic activities and microbial actions. Metabolites are subsequently
generated, increase or decrease in pH levels occurs and performance of Specifically for food safety, studies reported in the literature have
certain enzymes including proteases, amylases and hemicellulases is demonstrated fermentation as an effective and sustainable approach for
improved. These produced metabolites also inhibit and supress the the degradation and dissipation of pesticide residues (Kaushik, Satya, &
growth of pathogenic and spoilage microorganisms. Beyond its pre- Naik, 2009; Pinto, Castro, Miguel, & Koblitz, 2019), reduction/removal
servative effects, fermentation improves palatability, nutritional profile of toxic metals (Zhai et al., 2019; Zhang et al., 2017), reduction of anti-
and confer desirable organoleptic characteristics that impact flavor, nutritive factors (Adebiyi et al., 2018; Adebo et al., 2018), removal of
texture and aroma. In addition to this is the extension of shelf life and mutagenic contaminants (Turbic, Ahokas, & Haskard, 2002) and my-
production of health beneficial constituents. The microbiology and cotoxin degradation (Adebo et al., 2017b; Adebo, Kayitesi, & Njobeh,
biochemistry of fermentation have been well documented in the lit- 2019), which will be discussed in the proceeding section of this review.
erature (Adebo et al., 2017a; Anagnostopoulos & Tsaltas, 2019; Longo & Some of these attributes have been attributed to metabolites produced
Sanroman, 2006; Tamang, 2010) with these studies indicating that during fermentation, activities of starter cultures, absorption and
endogenous microorganisms that are activated during fermentation and binding of contaminants onto the bacterial cell walls, utilization of
through subsequent activities produce several compounds that result in these contaminants as primary sources of carbon, phosphorus and ni-
the aforementioned changes. trogen and the production of enzymes responsible for the degradation

3
 Table 2
Documented studies on the effect of fermentation on mycotoxins.
Fermented food Raw material Mycotoxins investigated Mechanism of reduction/increase Analytical method Reference
product
J.A. Adebiyi, et al.

Amahewu Maize FB1, ZEA Physical binding by LAB HPLC (Mokoena, Chelule, & Gqaleni, 2005;
AFB1, FB1 and ZEA Degradation or conversion into an undetectable compound 2006)
Anti-mycotic and anti-mycotoxigenic potential Chelule, Mbongwa, Carries, and Gqaleni
(2010)
Doklu Maize AFT Noncovalent binding of mutagens by fractions of the cell wall skeleton of LAB HPLC Assohoun, Djeni, Koussémon-Camara,
Opening of AF lactone ring resulting in complete detoxification and Brou (2013)
Ergo Milk AFM1 Binding of the AFM1 with the trace levels of dead bacterial cells ELISA Shigute and Washe (2018)
Noncovalent binding with the chemical components of the bacterial cell wall
Fermented gruel Maize FB1 Production of acids (causing reduction in pH) and low molecular weight metabolites HPLC Nyamete, Mourice, and Mugula (2016)
contributed to reduction
Binding of mycotoxin to LAB cell wall and/or conversion of mycotoxin into less/non-toxic
derivatives
Fermented wort Wort DON, HT2, T2, DON3Glc, HT2+T2 Binding of toxins to yeast cells and biotransformation through acetylation, glucosylation LC-TQ-MS/MS Nathanail et al. (2016)
and sulfonation
Kefir Milk AFM1 Binding ELISA Sani, Marhamati, and Marhamatizade
(2014)
Kenkey Maize AFs No effect on AFs HPLC Jespersen, Halm, Kpodo, and Jakobsen
AFB1, AFB2, CIT No effect on CIT (1994)
Increase in AF – reformation of hydrolysed AF molecules, presence of AF precursors and (Kpodo et al., 1996)*
substances that stimulates AF production
Kunu Maize AOH, AME, BEAU, DON, ENN, FB1, LAB present during fermentation could have degraded mycotoxins, fermentation caused LC-MS/MS Ezekiel et al. (2015)
tFB, FP, MON, ZEN conversion of ZEN to less estrogenic form β-ZOL
Some mycotoxins are soluble in water and discarded as part of steeping supernatant

4
Kunu Maize 3-NPA, AFB1, AFB2, AFM1, AFTo, Steeping contributed to mycotoxin reduction LC-MS/MS Ezekiel et al. (2019)
AME, AOH, BEA, CIT, MON Binding of mycotoxins and/or degradation/biotransformation
Mawe Maize AFs, tFBs Less reduction might be attributed to presence of AF precursors in maize VICAM Fandohan et al. (2005)
Maize and AFB1 Steeping and fermentation processes (mechanism not specified) TLC Adegoke, Otumu, and Akanni (1994)
sorghum
Ogi Sorghum AFB1 Losses in overtail, wash water and AF degradation TLC Dada and Muller (1983)
Ogiri Melon seed AFB1, AFG1 Thermodynamically enhanced reactions between the AFs and other constituents of the TLC Ogunsanwo, Faboya, Idowu, Ikotun, and
seeds, acid-base attack on coumarin moiety. Reduced pH and microbial activity Akano (1989a)
Pito Sorghum BEAU, DON, tFB, MON, ZEN LAB present during fermentation could have degraded mycotoxins, fermentation caused LC-MS/MS Ezekiel et al. (2015)
conversion of ZEN to less estrogenic form β-ZOL
Some mycotoxins are soluble in water and discarded as part of steeping supernatant
Soy-ogi Soybean, Maize AFB1, AFG1 Actions of bacteria during fermentation, producing an acidic environment leading to an TLC Ogunsanwo et al. (1989b)
“attack” on the coumarin moiety of AFs
Ting Sorghum FB1, FB2, FB3, T-2, ZEA, α-ZOL, β-ZOL Breakdown and/or degradation of mycotoxins to less toxic products by the fermenting Adebo et al. (2019)
microbiota
Enhanced interaction between mycotoxins and LAB cell wall
Adsorption of mycotoxins onto LAB cell wall surface components
Wine Grape OTA Adsorption to cell wall HPLC Meca et al. (2010)
Wort Malt DON, T2 Ability of yeasts to absorb mycotoxin GC Garda et al. (2005)
Mycotoxin solubility in aqueous medium
Reduced extractability due to ability of mycotoxin to join soluble proteins
Humid heating during brewing process
Yoghurt Milk AFM1 Binding ELISA Adibpour et al. (2016)

* - document increase in mycotoxins; α-ZOL – alpha zearalenol; β-ZOL – beta zearalenol; 3NPA – 3-nitropropionic acid; AFB1, - aflatoxin B1, AFB2, - aflatoxin B2; AFs – total aflatoxin; AFG1 – aflatoxin G1; AFM1 – aflatoxin
M1; AFTo – aflatoxicol; AOH – alternariol; AME - alternariolmethylether; BEAU – beauvericin; CIT – citrinin; DON – deoxynivalenol; DON3Glc – deoxunivalenol-3-glucoside; ELISA – enzyme-linked immunosorbent assay;
ENN - enniatins (Sum of ENN-A and ENN-B); FB1 - fumonisin B1; FB2 - fumonisin B2; FB3 - fumonisin B3; FP – fusaproliferin; GC- gas chromatography; HPLC – high performance liquid chromatography; HT2 – HT-2 toxin;
LC-MS/MS – liquid chromatography tandem mass spectrometry; LC-TQ-MS/MS – liquid chromatography triple quadrupole tandem mass spectrometry; MON – moniliformin; T2 – T-2 toxin; tFB – total fumonisins (sum of
FB1, FB2 and FB3); TLC – thin layer chromatography; ZEA/ZEN – zearalenone.
Food Control 106 (2019) 106731
J.A. Adebiyi, et al.
of these contaminants. Dalie, Deschamps, and Richard-Forget (2010)
listed some of the metabolites known to contribute to this effect include
organic acids, phenolic compounds, proteinaceous compounds, hy-
droxyl fatty acids and reuterin. Further to these is the production of
antagonistic substances that are inhibitory to other microorganisms as
well as anti-fungal and anti-bacterial effects.
As earlier indicated in Section 2, mycotoxins are deleterious food
contaminants. The presence and harmful effects of these fungal sec-
ondary metabolites necessitate a sustainable and effective decontami-
nation technique that would not only positively influence the quality of
food, but also reduce or at best eliminate mycotoxins. Studies docu-
mented in the literature have generally demonstrated a reduction of
mycotoxins after food fermentation through transformation, detox-
ification, binding, degradation and decontamination. These available
studies have been summarized in Table 2.
Although a few of them, some studies have documented an increase
in mycotoxin levels after fermentation. A reformation and closing of the
lactone ring of AFs have been suggested as possible cause of increase in
AF levels during maize fermentation (Kpodo, Sorensen, & Jakobsen,
1996; Price & Jorgensen, 1985). The authors ascribe such mycotoxin
increase to pH reduction and the presence of organic acids, which
contribute to reformation of hydrolysed AF molecules yielding higher
AF levels (Fandohan et al., 2005; Kpodo et al., 1996). Same authors as
well as Zaika and Buchanan (1987) also posited that the presence of AF
precursors and other substances such as acetone, ethanol, DL-ethionine,
isoprothiolane, nisin, phytate and sodium chloride during food fer-
mentation can stimulate fungal growth and AF formation by aflatoxi-
genic fungi thereafter. Because this it worrisome, monitoring of these
substances in the food produce prior to fermentation is critical, as lower
levels of these constituents could translate to limited formation of
mycotoxins.
On the contrary, more studies in the literature have rather found
fermentation as an effective process for mycotoxin control. As docu-
mented in previous studies and summarized herein (Table 2), myco-
toxin control during fermentation occurs via various mechanisms,
which include modification of the chemical structure of the mycotoxin
molecule, removal or detoxification/inactivation, adhesion to bacterial
cell walls (Fig. 2) leading to reduced toxicity. Irrespective of the me-
chanism of reduction, an effective mycotoxin food decontamination/
detoxification process should ideally be irreversible, with non-toxic
decontamination/detoxification products, and the food retaining its
palatability and nutritive value thereof.
Although there are few studies investigating the palatability/nu-
tritive values of these fermented products, the broad mechanism of
mycotoxin reduction during fermentation can either be through binding
with yeast or LAB cells and/or degradation/dissociation/bio-conversion
of the mycotoxin molecule (Adebo et al., 2017b; Hassan, Zhou, &
Bullerman, 2015; Mishra & Das, 2003; Pfliegler, Pusztahelyi, & Pócsi,
2015; Shigute & Washe, 2018). According to previous authors (Garda
et al., 2005; Shetty & Jespersen, 2006; Taheur et al., 2019), fermenta-
tive organisms including yeasts and LABs are capable of adsorbing
mycotoxins from agricultural products onto their cell wall surface
components such as glucans, peptidoglycans, polysaccharides, gluco-
mannans, annanoligosaccharides, teichoic acids, thereby, effectively
decontaminating mycotoxins in food. While microorganisms can absorb
mycotoxins by attaching these toxins to their cell wall components or
by active internalization and accumulation, dead microorganisms can
equally absorb mycotoxins (Juodeikiene, Basinskiene, Elena Bartkiene,
& Matusevicius, 2012). This also informs the assertion that yeast and
LAB removal of mycotoxins is usually through adhesion to cell wall
components as opposed to covalent binding or metabolism, as dead
cells do not necessarily lose their binding ability (Baptista et al., 2004;
Dalie et al., 2010; Juodeikiene et al., 2012; Santin et al., 2003; Shetty &
Jespersen, 2006; Taheur et al., 2019). As such, the adoption of con-
trolled fermentation via the use of starter cultures which does effec-
tively reduce mycotoxins through improved acidification and
5
Food Control 106 (2019) 106731
metabolism, while improving product quality has been suggested for an
improved process (Adebo et al., 2017b, 2018, 2019; Benkerroum, 2013;
Kandasamy, Kavitake, & Shetty, 2018).
Regardless of the metabolism of respective microorganisms, the
extent and strength of this binding process is based on the interaction
between the toxin and functional groups of the cell surface and related
to complexation, ion exchange, physical adsorption and amino acid
composition of peptidoglycan structure as well as environmental con-
ditions (Adibpour, Soleimanian-Zad, Sarabi-Jamab, & Tajalli, 2016;
Bovo, Franco, Rosim, & Oliveria, 2014; Zoghi, Khosravi-Darani, &
Sohrabvandi, 2014). Excellent reviews documenting detailed interac-
tions of yeasts and LABs for decontamination of fermented foods are
available in the literature (Dalie et al., 2010; Juodeikiene et al., 2012;
Shetty & Jespersen, 2006; Taheur et al., 2019) and can be consulted for
further information.
Particularly in food fermentations, few studies have elucidated the
mechanism of decontamination and reduction of mycotoxins. During
the fermentation of soy-ogi, Ogunsanwo, Faboya, Ikotun, and Idowu
(1989b), indicated that the presence of bacteria in the fermenting slurry
of the soy-ogi must have led to the production of acids, which probably
provoked an attack on either the 2,3-position of the terminal furan ring
of the AF-molecule, or on the coumarin moiety. The authors further
indicated that due to the absence of AFB2 and AFG2, the attack was
rather on the coumarin moiety of the AF-molecule (Fig. 3), as opposed
to the 2,3-position of the terminal furan ring. Could this mean that AFB1
degradation during fermentation could lead to the production of less
toxic AFB2 and AFG2? While such was not observed in the literature
reviewed herein, it further reemphasizes the need for investigating the
toxicity of products after fermentation, such that degraded products
would not have toxicities similar or even more than the parent myco-
toxin.
According to Nathanail et al. (2016), binding to yeast cells was
implicated as the mode of mycotoxin removal during wort fermentation
with lager yeast (Saccharomyces pastorianus). This study also suggested
that the toxins were not only bound to the yeast surface, but also en-
tered the cells and potentially biotransformed. Through putative me-
tabolites identified on LC–QTOF–MS/MS, the authors indicated that the
derived metabolic products were formed through (de)acetylation, glu-
cosylation and sulfonation (Nathanail et al., 2016).
Such conversion of mycotoxins to much less toxic products during
fermentation such as the conversion of ZEN to its less estrogenic form,
β-zearalenol has been reported (Ezekiel et al., 2015; Mizutani,
Nagatomi, & Mochizuki, 2011). Fermenting microorganisms may also
enzymatically transform mycotoxins generally to less toxic compounds
or they can deconjugate modified forms present in raw materials
(Berthiller et al., 2013). Reduced extractability or the ability of some
mycotoxins to react with soluble proteins or other constituents could
also contribute to mycotoxin reduction (Garda et al., 2005).
As demonstrated in other studies, losses or reduction in mycotoxin
levels could also be due to additional processing steps/units operations,
prior to or after fermentation. Accordingly, water solubility of some
mycotoxins plays a huge role in this and has been demonstrated in
reported studies (Ezekiel et al., 2015; Zhang & Wang, 2015). Such ob-
servations made from these studies indicates the role of other food
processes in the reduction of mycotoxins and as such, should not be
disregarded in ensuring a safe and ‘mycotoxin-free’ product.
It should also be noted that the extent of mycotoxin reduction varies
in each food system. Not only is this due to the nature and composition
of the substrate (raw material), but can equally be attributed to dif-
ferences in the mycotoxin chemical structure, polarity, dissociation
constant as well as starting mycotoxin levels that subsequently influ-
ences the highlighted mechanisms of reduction. Furthermore, several
other compounds equally compete and have the capability of reacting
with the cell wall of fermenting strains, making them equal competitors
for mycotoxin detoxification process (Amezqueta, Gonzales Peñas,
Murillo-Arbizu, & Lopez de Cerain, 2009; Meca, Blaiotta, & Ritieni,
J.A. Adebiyi, et al.
mycotoxins to
cells of
Other processing microorganisms
steps before
through Mycotoxin
metabolites
Noncovalent
binding with cell
microorganisms
Fig. 2. A summary of mycotoxin reduction mechanisms in fermented foods.
O
HOOC
O
H+
OCH3
Fig. 3. Acid attack on the coumarin portion of aflatoxin during the production
of soy-ogi (Adapted from Ogunsanwo et al., 1989b).
2010). These include but not limited to carbohydrates, proteins, phe-
nolic compounds, vitamins and colloidal particles.
4. Conclusion and future prospects
While several techniques for mycotoxin control and management
prove rather costly and/or impracticable in some instances, fermenta-
tion is a viable process for mycotoxin reduction in the African continent
as well as other developing countries. This is due to its afordablabilty,
ease of the process as well as numerous other benefits the fermentation
process confers to food. In addition to fermentation are very much
needed food safety management systems that can improve the quality
of the final products, while ensuring protection of consumer health. In
this regard are tailored and validated HACCP plans that could be
adapted to identify critical control points during the production African
fermented foods. Fairly new food safety approaches of VACCP (vul-
nerability assessment critical control points), TACCP (threat assessment
critical control points) and HARPC (hazard analysis and risk-based
6
Food Control 106 (2019) 106731
Physical binding
microorganisms
ersion into an
undetectable
form
group responsible
for mycotoxin
toxicity
preventive controls) should also be explored and implemented to en-
sure an effective control system. Regular surveillance and monitoring of
mycotoxins, raising awareness on these toxins cannot also be over-
emphasized.
In addition to its other numerous benefits, fermentation is desirable
for mycotoxin reduction. However, detailed insights into the nature of
metabolites formed after fermentation as well as the toxicity of pro-
ducts formed after fermentation are vital. Concerted efforts by re-
searchers and scholars in this field should be directed towards pro-
viding such insights in addition to elucidating the mechanisms of
mycotoxin detoxification/reduction processes. This will not only pro-
vide the much needed clarity of this viable and sustainable process of
myctoxin detoxification, but also contribute to existing knowledge in
this domain.
Acknowledgement
This work was supported via the Global Excellence and Stature
(GES) Fellowship of the University of Johannesburg and the
Department of Science and Technology (DST) - National Research
Foundation (NRF), South Africa Innovation Scholarship granted to the
main author (Adebiyi, J.A). The European Union-NRF/LEAP-AGRI
funding is equally acknowledged.
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