Cereal-Based Fermented Foods of Africa as ... - Open Science

14 downloads 0 Views 681KB Size Report
Aug 30, 2015 - production of gruels which is used as complementary food for babies and ... present status of some indigenous cereal fermented foods and ...
International Journal of Microbiology and Application 2015; 2(4): 71-83 Published online August 30, 2015 (http://www.openscienceonline.com/journal/ijma)

Cereal-Based Fermented Foods of Africa as Functional Foods Ome Kalu Achi*, Michael Ukwuru Department of Microbiology, Michael Okpara University of Agriculture, Umudike, Abia State, Nigeria

Email address [email protected] (O. K. Achi)

To cite this article Ome Kalu Achi, Michael Ukwuru. Cereal-Based Fermented Foods of Africa as Functional Foods. International Journal of Microbiology and Application. Vol. 2, No. 4, 2015, pp. 71-83.

Abstract Fermented cereal foods play an important socio–economic role in developing countries as well as making a major contribution to the protein requirements of natural populations. In general, traditional fermented foods are made under primitive conditions, which result in low yield and poor quality. Their microbiota which is dominated by lactic acid bacteria has been extensively investigated. The relation between microbial diversity and product characteristics are linked between the food microbiota and health benefits. Functional foods, in addition to their basic nutrients, contain biologically active components, in adequate amounts, that can have a positive impact on the health of the consumer. These foods generally contain health-promoting components beyond traditional nutrients. The beneficial effects are the preservation of foods and the increase in their organoleptic characteristics because of the production of lactic acid and other metabolites synthesised by lactic acid bacteria. Cereals which include maize (Zea mays), Sorghum (Sorghum bicolor), millet (Peninsetum americanum) are used in the production of gruels which is used as complementary food for babies and serves as breakfast for adults. This paper outlines the present status of some indigenous cereal fermented foods and beverages with some information on the microbiology and biochemistry of the fermentations as well as the beneficial and their health attributes. Among these are ogi, a fermented cereal gruel used as a weaning food, pito and burukutu, alcoholic cereal beverages. The use of such foods as delivery vehicles for probiotic bacteria will be discussed.

Keywords Lactic Acid Bacteria, Cereal Fermented Functional Foods, Health Benefits

1. Introduction Fermentation of cereal based foods is a common practice in Africa for food preservation. It is a technology that is simple; home based and has fed millions of people. Currently, a variety of fermented foods are produced from cereals at house hold and semi industrial scale. These foods are used as weaning food for infants and children (Lei and Jacobsen 2004, Kalui et al., 2008) and also for adults. A wide range of cereal-based fermented foods and related processes is a testimony to cultural diversity and to the ability of humans to find ways to produce foods in different contexts. The beneficial effects are the preservation of foods and the increase in their organoleptic characteristics because of the production of lactic acid and other metabolites synthesised by lactic acid bacteria (Guyot, 2012). Cereals which include maize (Zea mays), Sorghum

(Sorghum bicolor), millet (Peninsetum americanum) and acha etc. are used in the production of gruels which is used as complementary food for babies and serves as breakfast for adults. Functional foods are defined as foods that, in addition to their basic nutrients, contain biologically active components, in adequate amounts, that can have a positive impact on the health of the consumer. These foods generally contain healthpromoting components beyond traditional nutrients (Berner and O′Donnell, 1998). Recently, people have realized that fermented foods have a role beyond provision of energy and body maintenance. Scientific investigation has shifted to research on the fermentation benefits (Kalui et al., 2010). Investigation has revealed that fermentation processes have been discovered to produce active substances (Grajek et al., 2005), flavour enhancing compounds, important enzymes and amino acids. Some fermentation microorganisms are known to produce

72

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

anti–microbial substances which lead to safe and long shelf life of food products (Corgan et al., 2007, Kalui et al., 2009; Kalui et al., 2008, Parvez et al., 2006, Steinkraus, 2002). Useful microorganisms which have health benefits are associated with fermentation. Predominant among these organisms are Lactic acid bacteria (LAB) which produce lactic acid during fermentation (Holzapfel and Schilinger, 2002; Shah, 2007). These organisms are generally regarded as safe (GRAS). People’s need for natural health enhancing foods is a reason for research development in functional foods. Many workers have undertaken research into the probiotic potentials of many fermented foods (Grajek et al., 2005, Reid 2008; Vasiljevic and Shah 2008). These foods contain bioactive substances that prevent the initiation, promotion and development of allergies and diseases (Sanders, 2003, Pisulewski and Kostogrys 2003; Pervez et al., 2006; Lei et al., 2008; Vasiljevic and Shah, 2008). Cereals are a major component of human food in Africa. Nutritional experts have paid attention to cereal based foods from maize, sorghum and millet sources. These cereals have high content of soluble non-starch polysaccharides such as beta glucan which has a health promoting role. Clinical and epidemiological studies indicating that beta glucan from barley or oat based products control cardio vascular disease in humans have been reported (Beck et al., 2010, Shimzu et al., 2008; Karmally et al., 2005; Keogh et al., 2003). Duchonova et al. (2013) suggested that the multiple beneficial effects of cereal can be exploited in different ways hence design of novel cereal foods or ingredients can be targeted at a specific population. Furthermore, cereals are good fermentable substrates for the growth of probiotic microorganisms (Kochova et al., 2011 and Kedia et al., 2007; Charalampopoulos et al., 2008). Cereals can be used as sources of non – digestible carbohydrates. This selectively stimulates the growth of colonic lactobacilli and bifidobacteria which act as probiotics (Charalampopoulos et al., 2002, Chavan and Kadam, 1989; Duchonova and Sturdik, 2010). Growth of lactic acid bacteria in cereal based fermentation has led to a variety of cereal-based fermented foods like burukutu, pito, ogi etc. Hence incorporating human – derived probiotic strains in cereal substrates under control conditions would produce essential health benefits. There is thus increasing awareness among consumers about the health benefit of diets with high fibre content. Cereal-based fermented food products contain bioactive ingredients like dietary and functional fibres. The aim of this review is to discuss some African cereal based fermented foods and their relevance in promoting health.

2. Cereal as Fermentation Substrate Cereals are excellent substrate for microbial fermentation. Relevant important factors that affect their use as substrate for the growth of probiotics include; Composition of cereal substrate

Processing method Substrate fermentation Growth capability of the organisms Rate of productivity of starter culture Probiotic strain stability during storage Sensory properties of the product Nutritional value of the product Many traditional fermented foods like Ogi (akamu), burukutu, pito etc are popular in Nigeria. Maize, sorghum and millet are popular substrates used for the production of many fermented foods. These cereal grain physiologies indicate that they consist of embryo and endosperm which is enclosed by epidermis and covered by a seed coat or husk. The starchy endosperm is made up of varying sizes of granules and contains the carbohydrate. The embryo contains amino acids, lipids, sugars, minerals, vitamins and a range of hydrolytic enzymes such as amylases. These enzymes hydrolyse starch and make them available for microorganisms in form of sugars. The seed coat contains pectin, minerals, cellulose, pentosans and some contain polyphenols. These grains are processed and fermented in various ways to obtain a range of products. In the fermentation processes, the grains are modified through various steps, resulting in grain biochemical changes within the endosperm reserve of the grain in the preparation for microbial activities usually lactic acid bacteria and yeasts. Through the synthesis and activities of a range of enzymes in the grain, fermentable sugars are produced. These enzymes may be endogenous or exogenous (Hammes et al., 2005). The type of organisms that is found in association with each type of fermentation depends on ecological parameters like temperature, pH, inoculums, size, and nature of cereal and propagation time. Hence, fermenting organisms are not readily substrate specific but are conditioned by the factors mentioned. Anti – nutrients such as enzyme inhibitors, tannins and polyphenols are present in cereals. During fermentation these anti – nutrients are removed and physicochemical properties are enhanced leading to bioavailability. Similarly, mycotoxins which are undesirable compounds in cereals are removed by fermentation. Cereals are deficient in lysine but rich in cysteine and methionine: A combination of cereal with legumes can augment the protein. Mature cereal grains have relatively low level of free sugars. However, that low sugar level supports the beginning of the fermentation process. The breakdown of starch to simple fermentable sugars such as maltose and glucose is supported by cereal endogenous enzymes, selected enzymes or added malt. Some moulds also produce amylolytic enzymes powerful enough for hydrolysis and liquefaction. LABs are also capable of breaking down and utilizing starch. Cereals also contain relatively high levels of minerals, vitamins, sterols and other growth factors that support microbial growth. Physiological compounds used in functional food systems are available in cereals.

International Journal of Microbiology and Application 2015; 2(4): 71-83

3. Functionality of Cereal Foods Functional foods are defined as foods that, in addition to their basic nutrients, contain biologically active components, in adequate amounts, that can have a positive impact on the health of the consumer (Berner and O’Donnell, 1998). Recently, research has shown that nutrition plays a critical role in the prevention of chronic diseases (Lopez–Varela et al., 2002). A food can be seen as functional if it has beneficial effect on target functions in the body. It must contribute to the prevention and reduction of risk factors for several diseases or enhance certain physiological functions beyond nutritional effects (Kwak and Jukes, 2001; Saikia and Deka, 2011). In recent years, cereals and its ingredients are accepted as functional foods because they provide dietary fibre, proteins, energy, minerals, vitamins and anti-oxidants required for human health. Arabinoxylan and β–glucan are example of such dietary fibres. β–glucan is a soluble fibre which has the ability to increase solution viscosity and possible rapid fermentation in the small intestine. β–glucan can delay gastric emptying, increases gastro intestinal transit time and luminal viscosity (Saikia and Deka, 2011). These characteristics of β–Glucan are associated with slowed nutrients absorption, replaced blood glucose and insulin level. Jenkins et al. (1995) posited that acetic, propionic and butyric acids produced by fermentation in the colon may influence the production of glucose and its utilization by peripheral tissues. Cereals also contain resistant starch carbohydrates, galacto - and fructo–oligosaccharides. Charalampopuolos et al. (2002) showed that cereals are good fermentable substrates for the growth of probiotic microorganisms. Cereals have been acclaimed to prevent cancer and cardiovascular diseases, reduces tumour, lowers blood pressure, limits the incidents of heart diseases, controls cholesterol level and rate of fat absorption, delays gastric emptying and supplies gastrointestinal health. The potential of cereal nutrients in the control of coronary heart disease is well known. These nutrients include fibre, vitamin E, selenium, folate, linoleic acid as well as phenolic acids with anti – oxidants properties. Rice: The bran of the rice contains phytonutrients, which has diseases – preventing ability and other health related benefits (Jariwalla, 2001). The brown rice contains much higher phenolic compounds than the polished ones. These phenolic compounds contain properties that prevent cancer (Hudson et al., 2000). Maize – maize is a good source of many nutrients such as thiamine (Vitamin B1), Pentothenic acid (Vitamin B5), Vitamin C, folate dietary fibre, phosphorous and manganese. The fibre and folate content of maize account for its contribution to heart health. Maize maintains homocysteine which is responsible for damage of blood vessels heart attack, stroke or peripheral vascular diseases. Cryptoxanthin, a natural carotenoid pigment in maize reduces the risk of lungs cancer by a reasonable percentage if consumed daily (Yuan, 2003). According to Adam and Liu (2002) maize has the highest free phenolic content among many cereals.

73

Phenolic has anti – oxidative effects due to direct free radical scavenging activity (Shaidi, 2000, Shahidi and Ho, 2007) Sorghum: sorghum has high fibre and iron contents. Its hull has much nutrients. It also has fairly high protein content. Sorghum contain 3 – Deoxy-anthranyamdins in large quantity in the bran which are structurally related to the anthocyanin pigments – a health promoting phytochemical (Awika, 2004) Millet: Millet seeds are rich in phytochemical and phytic acid which is believed to lower cholesterol, phytate on the other hand is linked to cancer reduction. Other advantages of fermented cereal-based foods are Improved nutritive value Removal of anti-nutrient compounds Enhanced bioavailability Removal of mycotoxins Removal of endogenous toxins, cyanogenic compounds Reduction in energy required for cooking

4. The Nature of Cereal Fermentations Grains during storage are metabolically inactive with very low water activity of less than 0.6 and moisture content of 9 12%. This low water activity prevents the growth of microorganisms. The grains enzyme at this state is not active. This is the resting stage of the grain. Addition of water to the grains makes them absorb water which ultimately stimulates the enzyme into action and growth of microorganisms. This process enables fermentation to start. This is followed by size reduction through milling and sometimes the use of specific microorganisms and enzyme actions. Addition of water influences several ecological factors rapidly. Water activity of the grain increases leading to respiration which lowers the redox potential and pH. The combined endogenous hydrolytic activities such as amylosis, lipolysis, proteolysis and physiological activities of microorganisms bring about fermentation. The organisms may be deliberately added or are environmental contaminants whose occurrence is by chance. From this point, series of changes occur within the grain matrix. An ecological niche of microorganisms builds up and is influenced by several environmental factors leading to microbial succession during fermentation. Fermentation of cereals is influenced by several variables which require control by using technological methods to obtain standard quality. These are: Length of fermentation Temperature and pH of fermentation Moisture content of grain at steep out Extent of grain size reduction Degree of activity / alcohol level Type of cereal Growth factor requirements Cereal nutrients Enzyme sources

74

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

Materials added to the fermenting substrate Buffering capacity Level; of hygiene and sanitation Quality of starter These parameters are sometimes difficult to control especially under rudimentary conditions which are obtainable in household and small–scale level. These variables play a prominent role in fermentation. For instance, nitrogen sources, other growth factors like vitamins differ in cereal grains. The microorganisms act on the carbohydrate breaking them into simple sugars which range from 0.5 – 3%. This is made possible by the activities of amylolytic enzymes that degrade the starchy endosperm leading to supply of free sugars. At the same time proteolytic activity releases peptides and amino acids. Cereal inhibitors affect hydrolytic activities of the microorganisms. Blandino et al. (2003) posited that the type of bacterial flora developed in each food fermentation depend on the water activity, pH, salt concentration, temperature and composition of the food matrix. Traditional fermentation depends majorly on chance inoculation which involves mixed culture of bacteria, yeasts or both. Common fermenting bacteria are Leuconostoc spp., Lactobacillus spp., Streptococcus, Pedicoccus, Micrococcus and Bacillus.

fermented cereal foods have been investigated (Muyanja et al., 2002, Lei and Jacobsen, 2004; Sawadogi-Lingani, 2007; Odunfa and Oyewole 1998; Nigatu 2000; Achi, 1990, Mugula et al., 2002). Studies of traditional cereal fermentation in many parts of the world reveal similar microorganisms as earlier outlined (Ampe et al., 1999a, b, Ben Omar and Ampe, 2000; Ben Omar et al 2000; Escalante et al., 2001) The fermentation dynamics, growth kinetics and physicochemical changes during fermentation of Ogi were studied (Omemu, 2011). The population of filamentous moulds such as Aspergillus niger, A. flavus, Rhizopus nigricans, Fusarium subglutinans and Penicillum citrinum were reported to have declined significantly until they were completely absent towards the end of fermentation. LAB and Yeasts population increased steadily during fermentation. Yeasts isolated include Saccharomyces cerevisiae, Rhodotorula graminis, Candida krusei, Candida tropicalis, and Geotrichum fermentum. Predominant LABs include Lactobacillus fermentum, L. plantarum, and L. brevis. Table 1. Cereal fermented foods and beverages, sources and the organisms involved. Source Maize/sorghum/millet

Product Ogi

Maize/sorghum/

Fura

Maize/sorghum/millet

Agidi

Maize/sorghum/millet

Kunun-Zaki

Sorghum/millet

Burukutu

Sorghum/millet

Pito

5. Microbiology of Cereal Fermentation Lactic acid bacteria are the most common organisms that ferment cereals. LABs for food fermentation in African is popular due to the beneficial role of preservation, enhanced nutritional value, detoxification, production of flavour and aroma. Four genera which are most predominant are Lactobacillus, Lactococcus, Leuconostoc and Pedicoccus (Salovaara, 2004). Other organisms are Corynebacterium, Saccharomyces cerevisiae and Streptococcus (Table 1). In addition, mould species such as Aspergillus, Penicillum, Fusarium and Cladosporium may be involved. The fermentation processes is by chance inoculation often initiated by mixed microbial population. The organisms are usually from the environment or from the previous reserved batch (backslopping). This inoculation and subsequent metabolic activities result in increasing acidity of the medium thus leading to the elimination of non-lactic acid microorganisms. Subsequent microbial succession inactivates or kills some organisms while others continue with the fermentation. Surviving lactic acid bacteria in the fermentation form a synergy with some yeasts. The fermentation is spontaneous as a result of competitive microbial activities. Hence some strains are best adapted with rapid growth thereby dominating others at particular stages of fermentation. This accounts for succession process as reported by many workers (Mbata et al., 2009). The situation described above also exists during backslopping when some starter cultures (co-culture) are used in some African fermented cereal foods. Dominating microorganisms in some

Microorganism Lactobacillus plantarum, Saccharomyces cerevisiae, Candida mycoderma, Corynebacterium Lactobacillus plantarum, Pedicoccus, Leuconostoc, Streptococus, Enterococcus, S. ccereviciae Pichia anomala, Candida species Pediococccus acidolactic Lactobacillus plantarum, L. acidophilus,Leuconostoc, Streptococcus, Bacillus Lactobacillus fermentum, Lactobacillus leichimani, Escherichia coli, Streptococcus species Acetobacter spp., Candida spp. Leuconostoc mesenteroides Saccharomyces cerevisiae, S.chaveleri Acetobacter spp., Candida species, L. mesenteroides, S. cerevisiae S. chaveleri

6. Starter Culture in Cereal Foods Using amylolytic lactic acid bacteria as starter culture offers an alternative by combining both amylase production and acidification in one microorganism (Santoyo et al., 2003). Pure yeast cultures have been shown to increase protein

International Journal of Microbiology and Application 2015; 2(4): 71-83

content of fermented cereal products. Lactobacilli are the predominant organisms involved in the fermentation of cereal based foods and beverages in Africa. Beneficial starter cultures are not usually used in traditional fermentation of cereal based products. The fermented foods have probiotic potentials due to the Lactobacillus species contained in them. There are reports of the quality of some African fermented product that have been enhanced using beneficial cultures (Nyanzi and Jooste, 2013). Ogi was enhanced with a lactic acid starter culture and the product was called Dogik. The starter cultures have antimicrobial activities against diarrhoeagenic bacteria. Blandino et al, (2003) and Onyango et al, (2004) also reported the presence of Lactotobacillus paracasei, a probiotic Lactobacillus in association with other LABs in Uji – a cereal fermented food. Nout, (1991) reported that Lactobacillus acidophilus which are probiotic were isolated from African fermented sorghum – based products. Nwachukwu et al, (2010) have studied the spontaneous fermentation of cereals (Maize, millet, sorghum) for the production of Akamu and kunun–zaki. They reported the presence of lactic acid bacteria such as Lactobacillus plantarum, L. pentosus, L. celboiosus, Pedicoccus pentosaceus and Leuconostoc mesenteroides. L. plantarum was shown to have potential of being a starter culture for the fermentation of maize for Akamu production.

75

staple of that region and serves as a weaning food for infants. The traditional preparation of Ogi (Fig 1) involves soaking of corn kernels in water for 1-3 days followed by wet milling and sieving to remove bran, hulls and germ (Odunfa, 1985). The pomace is retained on the sieve and later discarded as animal feed while the filtrate is fermented (for 2-3 days) to yield Ogi, which is sour, white starchy sediment. Ogi is often marketed as a wet cake wrapped in leaves or transparent polythene bags. It is diluted to a solid content of 5 to 10% and boiled into a pap, or cooked and turned into a stiff gel called “Agidi” or “eko” prior to consumption.

7. Traditional Cereal-Based Fermented Foods Indigenous fermented foods prepared from major cereals are common in Nigeria and many parts of Africa. Some are used as beverages, breakfasts or snack foods which a few are consumed as staples and weaning foods (Iwuoha and Eke, 1996; Egwim et al., 2013).

Fig. 2. Traditional method of processing Agidi.

Fig. 1. Flow diagram for the preparation of Ogi.

Ogi or Akamu: Ogi or Akamu is a porridge prepared from fermented maize, sorghum or millet in West Africa. It is a

The major organisms responsible for the fermentation and nutritional improvement of Ogi include Lactobacillus plantarum, Corynebacterium, Aerobacter, the yeasts Candida, Mycoderma, Saccharomyces cerevisiae and Rhodotorula. Others include moulds like Cephalosporium,. Fusarium, Aspergillus and Penicillium species. Odunfa, (1985) observed that L. plantarum was the predominant organism in the fermentation responsible for lactic acid production. Corynebacterium hydrolysed corn starch to organic acids while S. cerevisiae and Candida mycoderma contributed to flavour development. Agidi: Agidi is a gel-like traditional fermented starchy food item produced from maize (Zea mays), although millet and sorghum can also serve as raw materials. Its colour depends

76

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

on the cereal used. It is cream to glassy white from maize, light brown from sorghum and grey to greenish colour from millet. It is known by different names in different localities such as “eko” (Yoruba), “akasan” (Benin), “komu” (Hausa) and “Agidi” (Ibo). It is becoming very popular, with acceptability cutting across the various multi-ethnic groups and socio-economic classes. The ease of consumption alone or with soup, stew, bean cake (akara), moi-moi, as light meal especially amongst post-operative patients and other patients in the hospitals makes it very popular (Ogichor et al., 2005; Dike and Sanni, 2010).

Fig. 3. Flow diagram for production of Fura.

Maize grains are sorted and cleaned, washed with clean water, soaked in clean water for 24-48 h, drained and wet milled using a commercial milling machine. This is followed

by wet sieving with the aid of a clean muslin cloth. The mixture is allowed to settle and the Ogi slurry supernatant decanted, boiled and cooked with occasional stirring to get agidi meal (Fig 2). The fermentation process in the traditional production of agidi was reported to have involved the activity of lactic acid bacteria and yeasts. Pediococcus acidilactici produced the highest quantity of lactic acid after 48 h followed by Lactobacillus plantarum while the Lactobacillus acidophilus produced the least lactic acid (Ogichor et al., 2005; Dike and Sanni, 2010). FURA: Fura is an example of an indigenous fermented cereal based foods – a popular drink in Northern Nigeria. It is a traditional thick dough ball snack produced principally from millet or sorghum and spices (ginger, pepper, black pepper and cloves). This food is prepared like “tuwo” and made into balls and eaten by many people. It can also be served as a combination dish known as “fura-de-nono which consists of millet balls and milk, and is a popular breakfast in northern Nigeria. (Jideani et al., 1999, 2001; Nkama and Gbenyi, 2001). The cereal grains (Millet or sorghum) are soaked in water overnight in a calabash so as to ferment. The soaked seed is drained and spread on a mat to dry in the sun. It is ground into a fine powder and stirred in boiled hot water until a smooth paste is formed. The paste is moulded into balls and is left for 1-4 days at room temperature to ferment, after which the balls are pounded and moulded before sun drying. The dried balls are then dry-milled into powder which can be reconstituted with water to get fura meal (Inyang and Zakari, 2008) (Fig. 3). The fermentation process in Fura is also induced by lactic acid bacteria (LAB) and yeasts. The lactic acid bacteria isolated from fura processing includes members of the genera Lactobacillus, Pediococcus, Streptococcus, Leuconostoc and Enterococcus. The most commonly isolated species is L. plantarum (Olasupo et al., 1997). Some of the lactic acid bacteria isolated during fura were able to hydrolyse starch. Nche et al. (1994) reported that Pediococcus species predominated in the latter stage of the fermentation. Among the yeasts isolated was Issatchenkia orientalis which dominated in fura processing, followed by Saccharomyccs cerevisiae, Pichia anomala and other Candida spp. NDALEYI: Ndaleyi is a fermented pearl millet food which is popular in Borno state, Nigeria (Nkama et al; 1994). Ndaleyi production is similar to the production of Ogi from millet or sorghum except that the grains are steeped for longer time.

8. Traditional Cereal-Based Fermented Beverages There are several types of cereal-based fermented drinks produced around the world, which can be classified based on the raw materials used or the types of fermentation involved

International Journal of Microbiology and Application 2015; 2(4): 71-83

in the production process. Kunun-zaki: This is a millet-based non-alcoholic fermented beverage widely consumed in the Northern parts of Nigeria. This beverage is however becoming more widely consumed in southern Nigeria, owing to its refreshing qualities. Adeyemi and Umar, (1994), described the traditional process for the manufacture of Kunun-zaki. This process involves the steeping of millet with spices (ginger, cloves, and pepper), wet sieving and partial gelatinization of the slurry, followed by the addition of sugar, and bottling (Fig. 4). The fermentation which occurs briefly during steeping of the grains in water over 8 - 48 h period is known to involve mainly lactic acid bacteria and yeasts. Sopade and Kassum, (1992), highlighted the significance of rheological characteristics in processing, quality control, sensory evaluation and structural analysis of Kunun-zaki. Increasing temperatures reduced viscosity but did not alter the rheological characteristics of the product. The time of shear (up to 1 h) did not appreciably alter the viscosity. Storage studies conducted by Adeyemi and Umar, (1994) revealed that the product has a shelf life of about 24 h at ambient temperatures, which was extended to 8 days by pasteurization at 60OC for 1 h and storage under refrigeration conditions. Studies are currently underway at the Federal Institute of Industrial Research Oshodi (FIIRO) Lagos, Nigeria to produce Kunun-zaki of improved shelf-life. FIIRO has been able to preserve Kunun-zaki effectively for 90 days with the use of chemical preservatives.

Fig. 4. Flow chart for the traditional process of Kunu-zaki.

Burukutu: This is a popular alcoholic beverage with vinegar like flavour, consumed in Northern Guinea Savanna region of Nigeria, in the Republic of Benin and in Ghana.

77

The preparation of Burukutu involves steeping sorghum grains in water overnight, following which excess water is drained. The grains are then spread out onto a mat or tray, covered with banana leaves and allowed to germinate. During the germination process, the grains are watered on alternate days and turned over at intervals. Germination continues for 4-5 days until the plumule attains a certain length. The malted grains are spread out in the sun to dry for 1-2 days, following which the dried malt is ground into a powder. Gari, (a farinaceous fermented cassava product) is added to a mixture of the ground malt and water in a ratio of one part gari to two parts malt and six parts water. The resulting mixture is allowed to ferment for 2 days, then boiled for approximately 4 h and allowed to mature for a further 2 days. The resulting product is a cloudy alcoholic beverage. Sorghum malt contains primarily yeasts and moulds as the indigenous microflora. Microorganisms associated with the fermentation include yeasts mainly Sacchromyces cerevisiae and S. chavelieri and the bacteria are Leuconostoc mesenteroides. The pH of the fermenting mixture decreases from about 6.4 to 4.2 within 24 h of fermentation and decreases further to 3.7 after 48 h. At the termination of the 2-day maturing period, Acetobacter spp and Candida spp are the dominant microorganisms. Boiling prior to maturation eliminates lactics and other yeasts. Fully matured burukutu beer has an acetic acid content which varies between 0.4 and 0.6%. Pito: Pito is the traditional beverage drink of the Binis in the mid-western part of Nigeria. It is now very popularly consumed throughout Nigeria due to its refreshing nature and low price. Pito is also widely consumed in Ghana. The preparation of pito involves soaking cereal grains (maize, sorghum or a combination of both) in water for 2 days, followed by malting and allowing them for 5 days in baskets lined with moistened banana leaves. The malted grains are ground mixed with water and boiled. The resulting mash is allowed to cool and later filtered through a fine mesh basket. The filtrate thus obtained is allowed to stand overnight, or until it assumes a slightly sour flavour, following which it is boiled to a concentrate. A starter from the previous brew is added to the cooled concentrate which is again allowed to ferment overnight. Pito, the product thus obtained, is a dark brown liquid which varies in taste from sweet to bitter. It contains lactic acid, sugars, and amino acids and has an alcohol content of 3%. Organisms responsible for souring include Geotrichum candidum and Lactobacillus spp. while Candida sp. is responsible for the alcoholic fermentation. Otika: ‘Otika’ is an alcoholic beverage traditionally brewed from sorghum malt and drunk in some parts of Nigeria. The production method is thus; grains of the red variety of guinea corn or sorghum are malted. Mortar and pestle are used to mill the malted sorghum into flour. The flour is suspended in water and boiled for at least 3 h, cooled and filtered. The filtrate is left at the prevailing room temperature to ferment for 3 days (or it may be inoculated with liquor from a previous ferment). The fermented

78

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

beverage is again filtered using ‘Ogi’ sieve cloth prior to consumption.

9. Functionality of Lactic Acid Bacteria in Cereal – Based Fermented Foods and Beverages Lactic acid fermentation of cereals is an age long processing method in Africa for the production of various foods and beverages. During fermentation the pH decreases with a simultaneous increase in acidity, accumulation of lactic acid and other organic acids due to microbial activity (Kohajdova and Karovicova, 2007). Unfermented cereals of foods lack flavour and aroma but when fermented, several volatile compounds are formed. These contribute to a complex blend of flavours and aroma which make products appealing. The production of organic acid by LAB during cereal fermentation is a major anti – microbial factor. This activity of LAB decreases the pH of the foods where they proliferate. LAB, in addition to organic acid, produces bacteriocins, carbon dioxide, ethanol, hydrogen peroxide and diacetyl. These factors contribute in ensuring the safety of fermented cereal foods and beverages. In spite of these, organic acid is considered to play a primary role while others play a secondary role (Adams, 2001). Bacteriocins are generally active against Gram – positive cells and not Gram – negative cells. This is because bacteriocins target cytoplasmic membranes which in the Gram – negative bacteria the polysaccharide layer provide a protective barrier against bacteriocins activity (De Vuyst, and Leroy, 2007). Furthermore, the fermentation processes prevents the growth, survival and toxins production of many pathogenic organisms. The presence of organic acid in the medium is the major inhibitory effect. The degree of inhibition is dependent upon many factors which include the type of organism involved, the temperature of the medium, the level of the acids dissociated as well as buffering capacity of the food. Cereal-based fermented foods are weakly buffered thus easily achieve low pH (Ali et al., 2003, Mugula et al., 2002, Lei and Jakobsen, 2004). If LAB fermentation is efficient, the pH of the food will be below 4.0 which could inhibit the growth and survival of contaminating microorganisms. Carbon dioxide produced during fermentation creates an anaerobic environment and is toxic to some aerobes as it acts on the cell membranes reducing the pH within and outside the cell. Microorganisms are selectively sensitive to CO2 with moulds and oxidative gram negative bacteria being more susceptible than lactobacilli and yeast. The aerobic condition of carbon dioxide during fermentation reduces all susceptible organisms when fermentation is initiated. This condition helps microorganisms resistant to carbon dioxide thus they proliferate. LABs are catalase negative hence cannot degrade the hydrogen peroxide in the presence of oxygen. There is possibility of hydrogen peroxide accumulation during fermentation and could be inhibitory to some

microorganisms. Although, other enzymes present in the fermentation can break down hydrogen peroxide thereby preventing their accumulation. This is why the contribution of hydrogen peroxide as antibacterial is still not clear (Kullisaar et al., 2002). Lactic acid fermentations have been reported to significantly inhibit mould growth and subsequent mycotoxin production (Ben Omar and Aupe, 2000). Where mycotoxins are produced ahead of lactic acid in fermentation, the toxin removal is difficult and remains in the product, hence a major risk. There are however, reports of mycotoxins degradation during cereal fermentation (Adegoke et al., 1994, Moss 2001). Enzymatic degradation or inactivation of mycotoxins have been suggested (Teniola et al., 2005; Alberts et al., 2006) or by binding of mycotoxins to the fermenting microorganisms (Haskard et al., 2000, El-Nezemai et al., 2001; Peltonen et al., 2001; Shethy and Jespersen, 2006). Yeasts resist and survive lactic acid environment during fermentations. Yeast species have a pattern of succession where by many yeast species are initially present during fermentation which progressively reduce to only few at the end of fermentation (Jespersen, 2003) LABs have several beneficial physiological effects such as antimicrobial activity, enhancing of immune potency (Kulhsaar et al., 2002) and prevention of cancer and lower serum cholesterol levels (Kaur, 2002). LABs also have bacteriostatic, bactericidal, viricidal, antileukemic and anti tumour effects in the consumer (Iwuoha and Eke, 1996) (Table 2). Table 2. Proposed health and nutritional benefits of lactobacillus species. Colonization and maintenance of suitable intestinal micro flora Enzyme formation Microbial interference and anti – microbial activities Competitive exclusion of undesirable microorganisms Clearance pathogens Reduction of removal of cholesterol Immuno - modulation and stimulation

The microbiota involved in many traditional African fermented cereal based food fermentation processes such as mawe (Hounhouigan et al., 1994), kenkey and ogi (Olasupo et al., 1997), Bushera (Muyanja et al., 2002), koko (Jakobsen and Lei, 2004) have lactic acid bacteria mainly of the genera Lactobacillus, Pediococcus, Leuconostoc and Enterococci. The microorganisms not only contribute to the flavor of the food but are also able to inhibit pathogenic and spoilage microorganisms through the various interactions as discussed earlier. Many strains produce bacteriocins and bacteriocinlike molecules that display antibacterial activity (Servin, 2004). In addition, it has been shown that some strains of LAB possess interesting health-promoting properties one of which is the potential to combat gastrointestinal pathogenic bacteria such as Helicobacter pylori, Escherichia coli (Leroy and De Vuyst, 2004). Fermented food containing live cultures called probiotics are considered as fermented functional foods. Probiotics, when consumed in adequate

International Journal of Microbiology and Application 2015; 2(4): 71-83

numbers, provide a health benefit directly or indirectly by production of metabolites to the host. The recognition of the beneficial effects of traditional fermented foods made of cereals containing lactic acid bacteria as probiotics is increasingly gaining importance. Lactobacillus bulgaricus and Streptococcus thermophillus are appropriate for rice fermentation since they have no amylase, which is necessary for saccharification of rice starch. In maize dough fermentation, L. plantarium and Pediococcus species dominate the latter stages being likely to be responsible for the rapid acidification of the inoculated dough.

10. Nutritional Value of Cereal - Based Foods Although spontaneous fermentation has preserved and improved the cereal based products for consumption, the use of starter culture is better. Opere et al. (2012) carried out a study on the indices of nutrition, palatability and preservation of ogi fermented from eleven cultivars of corn and sorghum using Lactobacillus pentosus and L. acidophilus in single and in combination as starter cultures during fermentation. The biochemical analysis of the samples showed concentration of acid, acetoin and diacetyl which increased compared to the control. They also had increased level of reducing sugars, proteins and amino acids. Essential amino acids, lysine, isoleucine and arginine were elicited in the fermented samples. Fermented samples also exhibited high level of inhibition on pathogenic and contamination microorganisms. Many cereal based foods are fermented and are major sources of inexpensive dietary energy and nutrients in Africa. In an effort to improve the nutritive value of sorghum ogi, Ajanaku et al. (2002) fortified the product with groundnut seeds (Arachis hypogea L.). A number of studies have been carried out to improve the nutritive value of ogi using fortification (Afolayan et al., 2010; Owuamanam et al., 2011; Egounlety et al., 2002). Cereal grains have adequate amount of sulphur containing amino acids, but relatively low in protein content especially in lysine. The protein of legumes could complement the protein of cereal grains in traditional fermented foods. Ogi is a popular Nigerian food with low biological value. Supplementation with 30% heated full – fat flour increases the protein.

11. Conclusion Many cereal-based fermented foods are excellent functional foods. They have beneficial effect on target functions in the body and contribute to the prevention and reduction of risk factors for many diseases. These cereals are good substrate for fermentation. Their fermentation is influenced by factors which require control through technological means. Lactic acid bacteria and yeasts are the predominant microorganisms during their fermentation. The activities of lactic acid bacteria during fermentation

79

contribute significantly to the production of many antimicrobials and inhibitory substances while the yeast contributes to flavour enhancement. The numbers of traditional foods which are considered here to be functional are actually natural whole foods. Therefore, these foods can be used as templates for innovation, where traditional starter cultures can be replaced by probiotic ones (Singh et al., 2014). Information about their health qualities can be used to proclaim benefits. Farnsworth (2004) pointed out the potential of root crops, legumes, shrimp, cassava, different types of vegetable flours, fish, fruit seeds, meats, fungi-based substrates, as well as milk from a variety of animals for the development of new probiotic foods. Application of probiotic cultures in traditional products represents a great challenge (MatillaSandholm, 2002). It is important that the formulation maintains the activity and viability of the probiotic for extended periods of time (Shah, 2007).

References [1]

Achi, OK. (1990). Microbiology of Obiolor – a Nigerian fermented non-alcoholic beverage. Journal of Applied Bacteriology, 69, 321-325.

[2]

Adams, MR. (2001). Why fermented foods can be safe. In: Fermentation and food safety. Adams, M.R. and Nout, MJR. (eds.). Aspen Publishers, Inc., Gaithersburg, Maryland, USA.

[3]

Adegoke, GO., Otumu, EJ and Akanni, AO.(1994). Influence of grain quality, heat, and processing time on the reduction of aflatoxin B1 levels in 'tuwo' and 'ogi': two cereal-based products. Plant Foods for Human Nutrition, 45, 113-117.

[4]

Adeyemi, IA. and Umar, S. (1994). Effect of method of manufacture on quality characteristics of Kunun-Zaki, a millet based beverage. Nigerian Food Journal, 12: 34 – 42.

[5]

Adom KK. and Liu RH (2002). Antioxidant activity of grains. Journal of Agricultural and Food Chemistry, 50 (21): 61826187.

[6]

Afolayan, MO; Afolayan, M and Abuah, JN (2010). An investigation into sorghum based ogi (Ogi-Baba) storage characteristics. Advance journal of Food Science and Technology, 2: 72 – 78.

[7]

Ajanaku, KO, Ajanku, CO; Edobo-Osoh, A and Nwinyi, OC (2012). Nutritive value of sorghum ogi fortified with groundnut seed (Arachis hypogae L). American Journal of Food Technology, 7(2): 82 – 88.

[8]

Alberts, JF, Engelbrecht, Y., Steyn, PS., Holzapfel, WH. and Zyl, WH (2006). Biological degradation of aflatoxin B1 by Rhodococcus erythropolis cultures. International Journal of Food Microbiology, 109, 121-126.

[9]

Ali, MAM., El Tinay, AH and Abdalla, AH (2003). Effect of fermentation on the in vitro protein digestibility of pearl millet. Food Chemistry, 80: 51-54.

[10] Ampe, F., ben Omar, N., and Guyot, JP. (1999a) Cultureindependent quantification of physiologically-active microbial groups in fermented foods using rRNA-targeted oligonucleotide probes: Application to pozol, a Mexican lactic acid fermented maize dough. Journal of Applied Microbiology, 87: 131-140.

80

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

[11] Ampe, F., ben Omar, N., Moizan, C., Wacher, C., & Guyot, J. P. (1999b) Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentations. Applied and Environmental Microbiology, 65: 5464-5473. [12] Awika, JM., Rooney, LW and Waniska, RD (2004). Properties of 3-deoxyanthocyanins from Sorghum, Journal of Agricultural and Food Chemistry, 52 (4): 4388-4394. [13] Beck, E.J; Tapsell, LC; Batterham, MJ; Tosh, SM and Huang, XF (2010). Oat betaglucan supplementation does not enhance the effectiveness of energy-restricted diet in overweight women. British Journal of Nutrition, 103(8): 1212 – 1222. [14] ben Omar, N. and Ampe, F. (2000) Microbial community dynamics during production of the Mexican fermented maize dough pozol. Applied and Environmental Microbiology, 66: 3664-3673.

[26] Egaunlety, M; Aworh, OC; Akingbala, JO; Houben, JH and Nago, CM (2002). Nutritional and sensory evaluation of maize-based tempe-fortified weanig foods. International Journal of Food Science and Nutrition, 53: 15 – 27. [27] Egwim E. Amanabo M., Yahaya A. and Bello M. (2013). Nigerian Indigenous Fermented Foods: Processes and Prospects, Mycotoxin and Food Safety in Developing Countries,. H Makun (Ed.), ISBN: 978-953-51-1096-5, InTech, DOI: 10.5772/52877. Available from: http://www.intechopen.com/books/mycotoxin-and-foodsafety-in-developing-countries/nigerian-indigenousfermented-foods-processes-and-prospects. [28] El-Nezami, H., Salminen, S. and Mykkanen, H. (2001). Binding of Aspergillus and Fusarium toxins by probiotic bacteria. Toxicology, 164: 175. [29] Escalante, A., Wacher, C and Farres, A. (2001). Lactic acid bacterial diversity in the traditional Mexican fermented dough pozol as determined by 16S rDNA sequence analysis. International Journal of Food Microbiology, 64: 21-31

[15] ben Omar, N., Ampe, F., Raimbault, M., Guyot, JP and Tailliez, P. (2000) Molecular diversity of lactic acid bacteria from cassava sour starch (Colombia). Systematic and Applied Microbiology, 23: 285-291.

[30] Farnworth, ER. (2004). The beneficial health effects of fermented foods—potential probiotics around the world. J. Nutraceut. Funct. Med. Foods, 4: 93–117.

[16] Berner, LA., O’Donnell, JA. (1998).Functional foods and health claims legislation: application to dairy foods. International Dairy Journal 8, 355-362.

[31] Grajek W, Olejnik A, Sip A (2005). Probiotics, prebiiotics and antioxidants as functional foods. Acta Biochimica Polonica. 52: 665-671.

[17] Blandino A., Al-Aseeri ME., Pandiella SS., Cantero D and Webb, C (2003). Cereal-based fermented foods and beverages. Food Research International; 36(6): 527-543.

[32] Guyot J-P (2012). Cereal-based fermented foods in developing countries: ancient foods for modern research. International Journal of Food Science and Technology,47, 1109–1114

[18] Charalampopoulos, D; Wang, R; Pandiella, SS and Web, C (2002). Application of cereals and cereal components in functional foods. International Journal of Food Microbiology, 79(1-2): 131 – 141.

[33] Hammes, PW; Brandt, JM; Francis, LP; Rosenham Sheltter, HFM, Vogeimann, AS (2005). Microbial ecology of cereal fermentations. Trends in Food Science and technology, 16: 4 – 11.

[19] Charalampopoulos, D, Vasquez, JA and Pandiella, SS (2009). Modelling and validation of Lactobacillus plantarum fermentations in cereal-based media with differrent sugar concentrations and buffering capacities. Biochemical Engineering Journal, 44: 96 – 105.

[34] Haskard, C., Binnion, C and Ahokas, J (2000). Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. Chemico-Biological Interactions, 128: 39-49.

[20] Chavan, JK and Kadam, SS (1989). Critical reviews in food science and nutrition. Food Science, 28: 348 – 400. [21] Corgan, TM. Bresford, TP, Steele, J. Broadbent J, Shah NP and Ustunol, Z (2007). Advances in starter cultures. Journal of Dairy Science. 90: 4005-4021.

[35] Holzapfel, WH and Schillinger, U. (2002) Introduction to pre- and probiotics. Food Research International, 35: 109116.

[22] De Vuyst, L Leroy, F,( 2007). Bacteriocins from Lactic Acid Bacteria: Production, Purification, and Food Applications. J Mol Microbiol Biotechnol;13:194–199

[36] Hudson, E.A; Dinh, P.A; Kokubar, T, Simmonds, MS and Gescher, A (2000). Characterization of potentially chemopreventive phenols in extracts of brown rice that inhibit the growth of human breast and colon cells. Cancer Epidemiology, Biomarkers and Prevention: a publication of the American Association of Cancer Research, 9(11): 1163 – 1170.

[23] Dike, KS and Sanni, AI. (2010). Influence of Starter Culture of Lactic acid bacteria on the Shelf life of ‘Agidi’, an indigenous fermented cereal. African Journal of Biotechnology, 9(46): 7922 – 7927.

[37] Inyang, C.U. and Zakari, U.M. (2008) Effect of germination and fermentation of pearl millet on proximate chemical sensory of instant fura – A Nigeria cereal food. Pakistan Journal of Nutrition, 7(1): 9 - 12.

[24] Duchonova, L; Polacovicova, P; Rakicka, M and Sturdik, E. (2013). Characterization and selection of cereals for preparation and utilization of fermented fiber-betaglucan products. Journal of Microbiology, Biotechnology and Food Sciences, 2: 2187 – 2207.

[38] Iwuoha C.I., Eke OS (1996).. Nigerian indigenous fermented foods: their traditional process of operation, inherent problems, improvements and current status. Food Research International, 29(5/6): 527-540.

[25] Duchonova, L and Sturdik, E (2010). Cereals as basis of preventing nutrition against obesity. Potravinaisto, 4: 6 – 15.

[39] Jariwalla, R.J (2001). Rice-bran products: Phyto-nutrients with potential applications in preventive and critical medicine. Drugs under Exp. Clinical Res., 27(1): 17 – 26.

International Journal of Microbiology and Application 2015; 2(4): 71-83

[40] Jenkins, D.J.A., Jenkins, A.L., Wolever, TMS., Vuksan, V., Rao, AV., Thompson, LL. and Josse, RG.(1995). Dietary fibre, carbohydrates metabolism and diabetes, Dietary fiber in Health and Disease, Kritchevsky, D., Bonheld, C. and St. Paul, pp.137-145, Eagan Press. [41] Jespersen, L. (2003) Occurrence and taxonomic characteristics of strains Saccharomyces cerevisiae predominant in African indigenous fermented foods and beverages. FEMS Yeast Research, 3: 191-200. [42] Jideani, V.A, Nkama, I., Agbo, E.B and Jideani, I.A. (1999). Prediction of changes in color of ‘Fura” during Storage. Nigerian Food Journal 17: 141 – 51. [43] Jideani, VA, Nkama, I., Agbo, ED. and Jideani IA. (2001). Survey of Fura production in some Northern states of Nigerian. Plant Food for Human Nutrition. 56: 23 – 26. [44] Kalui CM, Mathara JM, Kutima PM, Kiiyukia C, Wongo LE (2008). Partial characterization and identification of lactic acid bacteria involved in the production of ikii: a traditional fermented maize porridge by the Kamba of Kenya. Journal of Tropical. Microbiology and Biotechnology, 4(1): 3-15. [45] Kalui, CM,. Mathara, JM and Kutima, PM (2010). Probiotic potential of spontaneously fermented cereal based foods – A review. African Journal of Biotechnology, 9(17): 2490-2498. [46] Kalui CM, Mathara JM, Kutima PM, Kiiyukia C, Wongo LE (2009). Functional characteristics of Lactobacillus plantarum and Lactobacillus rhamnosus from ikii, a Kenyan traditional fermented maize porridge. African Journal of Biotechnology, 8(17): 4363-4373. [47] Karmally, W; Mortez, MG, Palmas, W; Martinez, W; Branstetter, A; Ramkrishnan, R; Holleran, SF; Haffra, SM and Ginsberg, HN. (2005). Cholestrol lowering benefits of oat containing cereal in hispanic Americans. Journal of the American Dietetic Association, 105: 967 – 970. [48] Kedia, G; Wang, R; Patel, H and Pandiella, SS (2007). Use of mixed cultures for the fermentation of cereal-based substrates with potential probiotic properties. Process Biochemistry, 42: 65 – 70. [49] Keogh, GF; garth, JSC; Mulvey, TB; Mcardle, BH; Coles, GD and Monro, JA. (2003). Randomized crossover study of the effect of a highly β-glucan barley on cardiovascular disease risk factors in mildly hyper cholestorolemic men. American Journal of Clinical Nutrition, 78: 711 – 718. [50] Kockora, M; Gerekova, P; Petrulakova, Z; Hybenova, E; Sturdik, E and Valik, L (2011). Evaluation of fermentation properties of lactic acid bacteria isolated from sourdough. Acta chemical Slovaco, 4(2): 78 – 87. [51] Kohajdova, Z and Karovicova, J (2007). Fermentation of cereals for specific purpose. Journal of Food and Nutrition Research, 46: 51 – 57. [52] Kullisaar, T., Zilmer, M., Mikelsaar, M., Vihalemm, T., Annuk, H., Kairane, C. and Kilk, A. (2002) Two antioxidative lactobacilli strains as promising probiotics. International Journal of Food Microbiology, 72, 215-224. [53] Kwak, NS, and Jukes, DJ (2001). Functional foods. Part 2: The impact on current regulatory terminology. Food Control, 12: 109 – 117. [54] Lei,

V

and

Jakobsen,

M.

(2004)

Microbiological

81

characterization and probiotic potential of koko and koko sour water, African spontaneously fermented millet porridge and drink. Journal of Applied Microbiology, 96: 384-397. [55] Lei V, Friis H and Michaelsen KF (2008). Spontaneously fermented millet product as a natural probiotic treatment for diarrhoea in young children: An intervention study in Northern Ghana. International Journal of Food Microbiology, 110: 246-253. [56] Leroy F, and De Vuyst L.(2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15: 67–78. [57] Lopes-varela, S; Gonzalez-Gross, M and Marcos, A (2002). Functional foods from buchwheat. Critical Review in Food Science and Nutrition, 41(6): 451 – 464. [58] Marchand J., and Vandenplas Y. (2000).Microorganisms administered in the benefit of the host: myths and facts. European Journal of Gastroenterology and Hepatology 12(10), 1077-1088. [59] Matilla-Sandholm, T. Myllarinen, P. Crittenden, R, Mogensen, G. Fonden, R. and Saarela, M. (2002). Technological challenges for future probiotic foods. Int. Dairy J., 12: 173– 82. [60] Mbata, T.I; Ikenebomeh, MJ, and Alaneme, JC (2009). Studies on the microbiological, nutrient composition and antinutritional contents of fermented maize flour fortified with bambara groundnut (Vigna subterranean L). African Journal of Food Science, 3(6): 156 – 171. [61] Moss, M.O. (2001) Chemical hazards and their control: Toxins. In: Fermentation and food safety. Adams, M.R. and Nout, MJR. (eds.). Aspen Publishers, Inc., Gaithersburg, Maryland, USA. [62] Mugula, JK. Narvhus, JA. Sørhaug, T (2003). Use of starter cultures of lactic acid bacteria and yeasts in the preparation of togwa, a Tanzanian fermented food. International Journal of Food Microbiology, 83(3), 307-318. [63] Mugula, JK., Nnko, SAM., Narvhus, JA and Sorhaug, T. (2002) Microbiological and fermentation characteristics of togwa, a Tanzanian fermented food. International Journal of Food Microbiology, 80, 187-199. [64] Muyanja, CMBK., Narvhus, JA., Treimo, J and Langsrud, T. (2002). Isolation, characterisation and identification of lactic acid bacteria from bushera: a Ugandan traditional fermented beverage. International Journal of Food Microbiology, 80, 201-210. [65] Nche, PF., Nout. MJR and Rombouts, FM. (1994). The effect of Cowpea Supplementation on the quality of Kenkey, a traditional Ghanaian fermented food. Journal of Cereal Science 19: 191 – 197. [66] Nigatu, A. (2000) Evaluation of numerical analyses of RAPD and API 50 CH patterns to differentiate Lactobacillus plantarum, Lact. fermentum, Lact. rhamnosus, Lact. sake, Lact. parabuchneri, Lact. gallinarum, Lact casei, Weissella minor and related taxa isolated from kocho and tef. Journal of Applied Microbiology, 89: 969-978. [67] Nkama, I. and Gbenyi, DI. (2001). The effect of malting of millet and sorghum on the residual Phytate and Polyphenols in Dakuwara, Nigerian Cereal-Legumes Snack food J. Trop. Agric. Pp. 270 – 275.

82

Ome Kalu Achi and Michael Ukwuru: Cereal-Based Fermented Foods of Africa as Functional Foods

[68] Nkama, I. and Gbenyi, DI. (2001). The effect of malting of millet and sorghum on the residual phytate and polyphenols in Dakuwara, Nigerian cereal-legumes snack food. Journal of Tropical. Agriculture, 44: 270 – 275 [69] Nkama, I., Abbo, ES. and Igene, JO. (1994). Traditional Production and Chemical Composition of ‘Ndaleyi’. A Nigerian fermented Pearl Millet Foods. Plant Foods for Human Nutrition, 46, 109 – 116. [70] Nout MJR.(1991). Ecology of accelerated natural lactic fermentation of sorghum-based infant food formulas. International Journal of Food Microbiology, 12, 217-224. [71] Nwachukwu, E, Achi, OK and Ijeoma, IO (2010). Lactic acid bacteria in fermentation of cereals for the production of indigenous Nigerian foods. African Journal of Food Science and Technology, 1(2): 021 – 026. [72] Nyanzi, R and Jooste, PJ. (2012). Cereal-Based Functional Foods, Probiotics, E. Rigobelo (Ed.), ISBN: 978-953-510776-7, InTech, DOI: 10.5772/50120. Available from: http://www.intechopen.com/books/probiotics/cereal-basedfunctional-foods [73] Odunfa, SA. and Adeyele, S. (1985). Microbiological changes during the traditional production of “Ogi-baba”-a West African fermented Sorghum Gruel Journal of Cereal Science, 3. 173 – 180. [74] Odunfa, SA and Oyewole, OB (1998). African fermented foods. In: Microbiology of Fermented Foods Vol 2. (second edition), Wood, BJB. (ed.), Blackie Academic & Professional, London, UK, pp 713-752. [75] Ogichor, IS., Ekundayo, AO. and Okwu, GI. (2005). Shelf Stability of agidi produced from Maize (Zea mays) and the effects of sodium benzoate treatment in combination with low temperature storage. African Journal of Biotechnology, 4(7): 738 – 743. [76] Olasupo, NA., Olukova, DK. and Odunfa, SA. (1997). Identification of Lactobacillus species associated with selected African fermented foods. Z. Naturforsch, 5: 105 – 108. [77] Omemu, AM (2011). Fermentation dynamics during production of ogi, A Nigerian fermented cereal porridge. Report and Opinion, 3(4): 8 – 17. [78] Onilude, AA., Fagade, MM., Bello, T and Fadahunsi, IF. (2005). Inhibition of aflatoxin-producing Aspergilli by Lactic acid bacteria Isolates from Indigenously fermented cereal gruels. African Journal of Biotechnology, 4: 1404 – 408.

preferment liquor, temperature and duration of fermentation. American Journal of Food Technology, 6: 374 – 384. [83] Parvez S, Malik KA, Ah Kang S and Kim HY (2006). Probiotics and their fermented food products are beneficial for health. Journal of Applied. Microbiology, 100: 1171-1185. [84] Peltonen, K., El Nezami, H., Haskard, C., Ahokas, J.and Salminen, S. (2001). Aflatoxin B-1 binding by dairy strains of lactic acid bacteria and bifidobacteria. Journal of Dairy Science, 84: 2152-2156. [85] Pisulewski P and Kostogrys RB (2003). Functional properties of foods of animal origin and the methods of their assessment. Pol. Journal Food and Nutrition Science, 12/53, SI 1: 65-73. [86] Reid G (2008). Probiotics and prebiotics–progress and challenges. Int. Dairy J. 18: 969-975. [87] Salovaara, H. (2004) Lactic acid bacteria in cereal-based products. In: Salminen, S., Von Wright A eds. Lactic acid bacteria: microbiology and functional aspects. 3rd ed. New York: Marcel Dekker Inc. [88] Saikia, D and Deka, SC (2011). Cereals: from staple food to nutraceuticals. International Food Research Journal, 18: 21 – 30. [89] Sanders, M.E (2003). Probiotics: considerations for human health. Nutrition Review, 61: 91-99. [90] Santoyo, MC; Loiseru, G; Rodriguez Sanoja, R; and Guyot, JP. (2003). Study of starch fermentation at low pH by Lactobacillus fermentum ogi E1 reveals uncoupling between growth and α-amylase production at pH 4.0. International Journal of Food Microbiology, 80: 77 – 87. [91] Sawadogo-Lingani, V. L. (2007). The biodiversity of predominant lactic acid bacteria in dolo and pito wort for the production of sorghum beer. Journal of Applied Microbiology, 103: 765-777. [92] Servin, AL (2004). Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiolological Reviews, 28, 405–440 [93] Shah, NP (2007). Functional cultures and health benefits – A review. International. Dairy Journal, 17: 1262-1277. [94] Shahidi, F. and Ho CT., (2007). Antioxidant measurement and applications. ACS Symposium Series 956. American Chemical Society, Washington DC. [95] Shahidi F., (2000). Antioxidants in food and food antioxidants. Nahrung 44 (3): 158-163.

[79] Onyango C., Bley T. Raddatz H and Henle T. (2004). Flavour compounds in backslop fermented uji (an East African sour porridge). European Food Research and Technology, 218: 579-583.

[96] Shetty, P.H and Jespersen, L. (2006.) Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends in Food Science and Technology, 17: 48-55.

[80] Opere,B; Aboaba,OO; Ugoji, EO and Iwalokin,BA (2012).Estimation of nutritive value, organoleptic properties and consumer acceptability of fermented cereal gruel (Ogi). Advance Journal of Food Science and Technology, 4(1): 1 – 8.

[97] Shimizu, C; Kihara, M; Aeo, S; Araki, S; Ito, K and Hayashi, K. (2008). Effect of high β-glucan barley on serum cholesterol concentrations and visceral fat area in Japanese men. A randomized double blinded, placebo controlled trial. Plant Food for Human Nutrition, 63: 21 – 25.

[81] Otles, S and Cagindi, O (2006). Cereal based functional foods and nutraceuticals. Acta Sci Pol, Technol Aliment., 5(1): 107 – 112. [82] Owuamanam, CI, Ogueke, CC, Achinewu, SC and Barimaka, IS (2011). Quality characteristics of gari as affected by

[98] Singh, A. Kumar, M. Ghosh, M and A. Gangul (2014).Traditional Foods and Beverages as Delivery Vehicles for Probiotics In: Biotechnology Vol. 8: Novel Drug Delivery B. Singh and O P Katare eds. Studium Press LLC ISBN: 9781626990234

International Journal of Microbiology and Application 2015; 2(4): 71-83

[99] Sopade, PA. and Kassum, AL. (1992). Rheological characterization of Nigerian liquid and semi-liquid foods. Kunun-zaki and Kunun gyada. Nigerian Food Journal. 10: 23 – 33. [100] Teniola, OD., Addo, PA., Brost, .M., Färber, P., Jany, KD., Alberts, JF., van Zyl, WH., Steyn, PS. and Holzapfel, WH. (2005). Degradation of aflatoxin B1 by cell-free extracts of Rhodococcus erythropolis and Mycobacterium

83

fluoranthenivorans sp. nov. DSM44556. International Journal of Food Microbiology, 105: 111-117. [101] Vasiljevic T and Shah NP (2008). Probiotics. From Metchnikoff to bioactives. International Dairy Journal, 18: 714-728.