Comparative characteristics of solid-state and submerged fermentations.
The cassava plant is grown in tropical and subtropical countries, which represents, alongside with its by-products, an important source of food and feed. Hence, this plant has the capacity to promote the economic development of those countries and provide food security. However, cassava has some disadvantages due to the antinutrient compounds produced in its tissues. In addition, the cassava roots have a low protein content. Due to the economic and practical advantages, the solid-state fermentation (SSF) has been used as a cost-effective and efficient processing method to detoxify the cassava products and enrich them in nutrients. This chapter reviews the solid-state fermentation technique of cassava products for the production of valuable components for food and feed applications, microorganisms involved in this process, and key factors used to optimize the SSF process.
- anti-nutritional value
- nutritional value
- processing variables
- solid-state fermentation
Among all the antinutrients, hydrogen cyanide (HCN) is of great concern, the concentration of which is in cassava and its by-products are much higher than the World Health Organization (WHO) safe limit for human consumption (10 ppm) [8, 9]. Konzo is an irreversible neurological disease associated with intake of HCN . Therefore, a detoxification process is needed to reduce anti-nutritional levels in order to consume cassava safely. Solid-state fermentation (SSF) has been used as an economical and efficient processing method for enriching and detoxifying cassava and its by-products [11, 12]. Various process parameters such as particle size, moisture content, water activity, pH, the inoculum size, incubation time, concentration of nutrient supplementation, and temperature can affect the microbial growth, enzyme production, and formation of the product during the SSF process .
This chapter discusses fermented cassava products through solid-state fermentation for food and feed applications, as well as microorganisms involved in solid-state fermentation and the essential processing variables used to optimize the process.
2. Fermentation processes
Fermentation has been one of the most used technologies to improve the taste and sensory properties of food and continues to be one of the most widely used methods of preserving the food for a length of time [14, 15]. The cassava fermentation process is a strategy to improve nutritional value by enriching protein and detoxifying toxic and anti-nutritional compounds, in particular by reducing toxic cyanogenic glycosides to a safe level of consumption in cassava products as well as reducing post-harvest losses [16, 17, 18].
There are two kinds of fermentation, i.e., spontaneous (natural) fermentation and controlled fermentation. For the natural fermentation, the conditions are selected so that to produce the most suitable microorganisms for the production of growth by-products characteristic of a particular type of fermentation . The controlled fermentation is generally used when the natural fermentation is unstable or the bacteria are not able to grow. In this case, specific microbial strains, such as lactic acid bacteria (LAB), yeast, and fungal are isolated, characterized, and preserved for later use as starter cultures . Under optimal growth conditions, these cultures can be used as single or combined starter cultures. As a result, the quality of products and their organoleptic characteristics are well controlled and predictable [20, 21].
However, the fermentation process can be broadly categorized into submerged fermentation (involving soaking in water) and solid-state fermentation (without soaking in water) . The solid-state fermentation (SSF) technique has several advantages over submerged fermentation (SmF). However, the SSF has some constraints. Table 1 illustrates the advantages and disadvantages of SSF over SmF .
2.1 Solid-state fermentation and its application in cassava products
In recent years, the cassava population has developed numerous processing methods (soaking, boiling, drying, and fermentation) [24, 25, 26]. SSF is one of the promising processes of enriching protein and detoxifying of cassava products [27, 28, 29].
Fermented cassava products by SSF, such as flour, gari, starch, bread, and biomass contain high protein content that can either be consumed by humans or animals, replacing expensive, conventional protein sources in different parts of Latin America, Africa, and Asia . The major fermented cassava products by SSF can be derived from different parts of the cassava plant, such as roots, peels, and leaves.
2.1.1 Cassava roots
Cassava is grown in many developing countries for its roots as a primary source of carbohydrates and ranks third in the developing countries as the leading source of energy in human diets along with rice and wheat . World production of cassava is estimated at 277 million tons of fresh root in 2017 . Cassava root has several advantages compared to other crop roots, including high productivity, resistance to droughts and pests, flexible harvesting age, and it can be kept in the ground until they are needed . However, cassava root also has certain disadvantages; its tissues contain toxic compounds (a cyanogenic glycoside), low protein content (1% fresh root weight), and short shelf life of 1–3 days .
Food processing techniques have been used to convert cassava tubers into flour as an alternative way to preserve the roots after harvesting and then further use it for industrial and traditional purposes [35, 36]. Gari and flour are the most popular fermented food products from cassava roots by SSF. In West Africa, approximately 200 million people consume gari [37, 38]. Figure 1 shows the production of flour and gari under the solid-state fermentation .
The purpose of cassava root fermentation is to increase the low protein content from 2% to about 7% or more than the critical crude protein content . To achieve this goal, several solid-state fermentation techniques have been used. Raimbault et al.  reported the principle underlying the SSF procedure for the enrichment of cassava flour. This procedure led to the enrichment of crude protein from 1 to 18–20%, which improved between 1700 and 1900% after 30 h of fermentation. Oboh and Elusiyan  studied the effect of solid-state fermentation by
In addition, Oboh and Akindahunsi  investigated the effect of solid-state fermentation with
2.1.2 Cassava peels
Cassava wastes, such as peels and leaves and starch residues make up 25% of the total cassava plant . Cassava peel is the leading waste from the cassava plant, but its use is limited due to the high content of cyanide and fiber as well as low protein and therefore disposed of it after cassava processing into food or other industrial products [44, 45]. Many efforts have been made using SSF techniques to enrich the protein content and degrade the cyanide level of cassava peels for animal feed.
Bayitse et al.  studied protein enrichment of cassava residue using
Iyayi and Losel  also evaluated protein improvement of cassava peels using different types of microorganisms and fermentation time (
Ezekiel and Aworh  evaluated the effectiveness of SSF with
In another study by Ruqayyah et al. , the application of response surface methodology was used to optimize SSF conditions (moisture content, inoculum size, and pH) with
Oboh  investigated the effect of solid-state fermentation of cassava peel with a mixture of
|Parameter||Solid-state fermentation||Submerged fermentation|
|Substrates||Insoluble substrates (starch, cellulose, pectins, lignin)||Soluble substrates (sugars)|
|Aseptic techniques||Sterilization of steam and non-sterile conditions||Sterilization of heat and aseptic control|
|Temperature||Difficult temperature control||Easy temperature control|
|Water||Low water consumption||High water consumption|
|pH control||Difficult pH control||Easy control of pH|
|Industrial level||Relatively small scale, newly designed equipment is needed||The industrial level is available|
|Inoculation||Spore inoculation, batch process||Easy inoculation, continuous process|
|Contamination||Contamination risk of low-growth fungi||Contamination risk of single strain bacteria|
|Energy||Low consumption of energy||High consumption of energy|
|Equipment volumes||Low volumes and low equipment costs||High volumes and high equipment costs|
|Pollution (effluents)||No volumes of effluents||High volumes of effluents|
|Concentration/products||100/300 g/L||30–80 g/L|
|Composition||Fresh||Naturally fermented||Fermented with a mixed culture|
|Crude protein (%)||8.2 ± 0.1||11.1 ± 0.3||21.5 ± 1.2|
|Crude fiber (%)||11.7 ± 0.5||6.5 ± 0.5||11.7 ± 0.5|
|Fat (%)||3.1 ± 0.4||3.5 ± 0.2||2.1 ± 0.1|
|Ash (%)||6.4 ± 0.4||6.0 ± 0.2||7.2 ± 0.2|
|Carbohydrate (%)||64.6 ± 0.2||67.3 ± 0.4||51.1 ± 0.4|
|Moisture (%)||5.1 ± 0.3||5.7 ± 0.2||6.4 ± 0.4|
|Ca (ppm)||0.03 ± 0.00||0.03 ± 0.00||0.03 ± 0.00|
|Na (ppm)||00.04 ± 0.00||0.04 ± 0.00||0.04 ± 0.00|
|Zn (ppm)||0.01 ± 0.00||0.01 ± 0.00||0.01 ± 0.00|
|K (ppm)||0.05 ± 0.00||0.05 ± 0.00||0.05 ± 0.00|
|HCN (mg/kg)||45 ± 0.3||24 ± 0.2||6.1 ± 0.4|
2.1.3 Cassava leaves
Cassava leaves are an extremely rich source of proteins, vitamins, and minerals that exceed some of the other green vegetables [47, 48]. The production of cassava leaves is estimated at 10 tons of dry leaves per hectare, which has a similar yield with the roots . Cassava leaves are consumed in most Southeast Asian and African societies, such as Indonesia, Malaysia, Congo, Madagascar, and Nigeria [50, 51]. However, cassava leaves contain both nutritive (33.8–37.4% protein content) and anti-nutritional compounds [301.04–192.47 (mg/100 g) HCN content] . Boiling, soaking, steaming, drying the sun, drying the oven, and cooking are the most common methods for processing cassava leaves in African and Asian countries .
The origin of HCN in the cassava leaves is a two-step process [54, 55]. First, the linamarin, a cyanogenic glycoside, which represent 93% of cyanogenic glycosides found in cassava (7% is lotaustralin), is hydrolyzed by linamarase (a beta-glycosidase) into glucose and cyanohydrin. Then, in the second step, the cyanohydrin is decomposed, either enzymatically or not, to HCN and acetone. The nonenzymatic pathway depends on pH. At pH > 6, the HCN is liberated, but at an acidic pH (~5), the process is much lower, and the resulting HCN is therefore relatively lower in concentration. However, this approach did not assure full hydrolysis of cyanogens. The partial breakdown of the leaf cells only partially releases linamarase resulting in only a certain proportion of the cyanogenic compounds being converted to HCN. This implies that a proportion of the cyanogens remain present in the leaves after processing and resulting in the release of HCN directly into the human body upon consumption.
The conventional methods have been proven to be ineffective for lowering the cyanide content in cassava leaves to the safe limit, at the same time causing a significant loss of protein and essential nutrients, which is highly desired from the cassava leaves [56, 57, 58, 59, 60]. Hence, the establishment of a universally acceptable method that produces edible leaves with low cyanide level while maintaining maximum nutritional content is challenging and still far away from being established. Among the efforts made so far, Morales et al.  proposed a solid-state fermentation of cassava leaves, reducing the cyanide content while improving the nutritional value of the processed leaves. SSF was performed using
One of the essential criteria for the solid-state fermentation is the selection of an appropriate microorganism . Several research works have explored different types of microorganisms mainly fungi, yeasts, and bacteria, as well as different substrates to favor the metabolism of the microorganisms in SSF of cassava products. Examples of microorganisms associated with solid-state fermentation of cassava products for food and feed applications are summarized in Table 3.
|Cassava peels||Animal feed|||
|Cassava peels||Poultry feed|||
|Cassava pulp||Animal feed|||
|Cassava leaves||Animal feed|||
|Cassava pulp||Lactic acid production|||
|Cassava root||Cellulase production|||
|Cassava root||Cassava flour|||
|Cassava peel||Feed supplements|||
|Cassava starch and leaves||Lactic acid and ethanol productions|||
3. Environmental factors
The process control of the solid-state fermentation parameters is closely related to the metabolic regulation of microorganisms . Based on the metabolic needs of the fermentation microorganisms, the control of water activity, oxygen content, temperature, and pH are the main solid-state fermentation parameters . In the solid-state fermentation process, the water, gas, and heat caused by the growth microbes are the dominant factors that determine the environmental changes. The environmental factors can affect the microbial growth and formation of the product during the SSF process [75, 13]. Therefore, the physical-chemical parameters must be controlled.
3.1 Water activity and moisture content
The unique feature of solid-state fermentation is that there is almost no free water in the substrate . However, microorganisms can grow depending upon the water activity of the substrate [64, 75]. The growth of fungi and some yeast usually requires a water activity value between 0.6 and 0.7 . In addition to meet the microbial physiological requirements, the water content level plays a decisive role in the variation of the three-phase structure relating to water retention, permeability, and thermal conductivity. The degree of swelling in the SSF system was low at a lower moisture level and hence increased water stress reduces nutrient solubility. On the contrary, the higher level of humidity results in changes in substrates that reduce porosity, thus contributing to stickiness and reduced gas exchange [78, 79]. According to Grover et al. , the required moisture content should range between 60 and 80% for an efficient SSF system.
The fermentation temperature affects microbial growth, spore germination, and the formation of product . Heat generation in solid-state fermentation system is more problematic than in liquid fermentation. Due to poor heat conductivity and accumulation of metabolic heat in the material combined with substrate shrinkage and decreased porosity, gas convection is severely impeded. Previous studies showed that the significant resistance to heat transfer in solid-state fermentation was low conduction efficiency [82, 83].
Therefore, moisturizing is a common measure of temperature control. In addition, routine operations (e.g., forced ventilation and jacket cooling) all can solve these problems . The evaporative cooling is one of the main solid-state fermentation temperature control measures [85, 86]. In general, the aeration could reduce the temperature gradient of the medium . The forced ventilation can take away more than 80% of the heat generated from the substrate . From the current investigation, it is difficult to maintain the temperature at an ideal range in SSF system. To reach this aim, the main strategy used in large-scale solid-state fermentation is to combine ventilation and humidity .
3.3 Oxygen concentration
The gas environment is a critical factor that significantly affects the relative levels of biomass and the production of an enzyme . Oxygen uptake rate (OUR) and carbon dioxide production (CDPR) can be used to assess the state of the solid-state fermentation process. However, different microorganisms cause these assessments to vary. Ghildyal et al.  studied the impact of the gas concentration gradient on product yield in a tray solid-state fermentation bioreactor. The results showed that the variations of O2 and CO2 concentration gradients were visible, which severely affected product yield. The yield decreased when gradient increases. Gowthaman et al.  also studied the impact of gas concentration gradient on the product in a packing bed bioreactor. The results showed that the gas concentration gradient could be eliminated and the ability of mass transfer can be enhanced by forced ventilation, which increased enzyme activity.
3.4 pH value
In general, if the initial pH value of the medium is adjusted, the variations of pH value during the solid-state fermentation process need to be considered . During the fermentation process, the pH values change drastically. The reason is that organic acids including citric and lactic are secreted during the fermentation process, which decreases the pH . While the increase in pH was rationalized in terms of organic acid decomposition and protein degradation in the raw materials into amino acids and peptide fractions . The pH values are difficult to determine by conventional detection in SSF due to the low water content of the substrate. Nitrogen-containing inorganic salts (such as urea) are often used as sources of nitrogen to offset the pH variation in the fermentation process [91, 92].
In the study conducted by Ezekiel and Aworh  to evaluate the effect of pH on protein enrichment and soluble sugars of cassava peel by
The results discussed in this chapter highlighted the importance of the SSF technique applied to cassava to improve its nutritional value. The solid-state fermentation using microbial protein is beneficial for the reduction of cyanide contents while the content of protein and other nutrients is increased compared to those obtained by the conventional approaches, i.e., soaking, boiling, and drying. Thus, the SSF technique for processing cassava products is better suited for developing societies and rural communities in the African and Asian countries that do not have easy access to available protein sources.
The authors are thankful to the Ministry of Research, Technology and Higher Education of the Republic of Indonesia for its financial support to this project through the grant no. 849/PKS/ITS/2018.
Conflict of interest
The authors declare no conflict of interest.
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