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International Journal of Food Microbiology 75 (2002) 197 – 212 www.elsevier.com/locate/ijfoodmicro
Appropriate starter culture technologies for small-scale fermentation in developing countries
IBM/IHT, BFE, Haid-und-Neu-Strasse 9, D-76131 Karlsruhe, Germany Accepted 28 December 2000
Abstract Modern food biotechnology has moved a long way since ancient times of empirical food fermentations. Preservation and safeguarding of food are, however, still major objectives of fermentation. In addition, other aspects, such as wholesomeness, acceptability and overall quality, have become increasingly important and valued features to consumers even in developing countries where old traditions and cultural particularities in food fermentations are generally well maintained. Due to limitations in infrastructure and existing low technologies, rural areas in most developing countries have not been able to keep abreast of global developments toward industrialisation. At the same time, fermented foods play a major role in the diet of numerous regions in Africa and Asia. In many traditional approaches, the advantages of some form of inoculation of a new batch, e.g. by back-slopping or the repeated use of the same container (e.g. a calabash) is appreciated and generally practised. Still, the benefits of small-scale starter culture application as a means of improved hygiene, safety and quality control, in support of HACCP approaches, are not yet realised in small-scale fermentation operations. Approaches and considerations for the selection of pure cultures for small-scale, low-tech applications may differ in some respects from the large-scale industrial approaches practised since 100 years. Selection criteria should take account of the substrate, technical properties of the strain, food safety requirements and quality expectations. Lack of experience in the application of starter cultures in small-scale operations and under rural conditions presents a major obstacle but also an exciting challenge to food microbiologist and technologist. Culture preservation, maintenance and distribution demand special logistic and economic considerations. Quality, safety and acceptability of traditional fermented foods may be significantly improved through the use of starter cultures selected on the basis of multifunctional considerations, also taking into account the probiotic concept and possibilities offered for improved health benefits. D 2002 FAO-AGS. Published by Elsevier Science B.V. All rights reserved.
Keywords: Food preservation; Traditional fermentation; Functional properties; Lactic acid bacteria (LAB); Food safety; Selection criteria
1. Introduction 1.1. Food fermentation Together with drying and salting, fermentation is one of the oldest methods of food preservation. Its importance in modern-day life is underlined by the wide spectrum of fermented foods marketed both in
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followed by yeasts. Inoculation to improve process control 2. have been applied in food preservation for millennia and were elucidated through trial and error. be described as palatable and wholesome foods prepared from raw or heated raw materials. 1997). Experience has also shown that back-sloping. and probably originated from microbial interactions of an acceptable nature. some of. Those best adapted to the food substrate and to technical control parameters. processes initiated without the use of a starter inoculum. Various types of starter cultures and even backslopping are widely used in fermentation processes. a typical starter facilitates improved control of a fermentation process and predictability of its products (Holzapfel.1. material from a previous successful batch is added to facilitate the initiation of a new process.H. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 developing and industrialised countries. In numerous traditional processes. aroma. texture. which may be added to accelerate a fer- Initiation of a spontaneous fermentation process takes a relatively long time (24 – 48 h).3. on culture and on the commercial distribution and storage of food. texture and improved cooking and processing properties. accelerates the initial phase of fermentation and results in the promotion of desirable changes during the fermentation process. by virtue of their metabolic activities.e. Spontaneous fermentations.Edited by Foxit Reader Copyright(C) by Foxit Software Company. in general. organic acids) inhibitory to other contaminating microbes (e. not only for the benefit of preservation and safety. Bacteria typically dominate the early stages of fermentation processes. fermentation has had a major impact on nutritional habits and traditions. even in industrialised countries (Table 1). i. but also for their highly appreciated sensory attributes. with high risk . owing to their relatively high growth rate. Definitions A starter culture may be defined as a preparation or material containing large numbers of variable microorganisms. traditional skills have been developed for controlling technical parameters during fermentation processes. Through this practice of backslopping. visual appearance. aroma. Enzymes indigenous to the raw materials may play a role in enhancing these characteristics (Hammes. Through trial and error. Fermentation has enabled our ancestors in temperate and cooler regions to survive winter season and those in the tropics to survive drought periods. 198 W.2005-2007 For Evaluation Only. In addition. or the inoculation of raw materials with a residue from a previous batch. They are generally appreciated for attributes such as pleasant flavour. and also for their safety and traditional acceptability. 2. 2. by improving the shelf life and safety of foods.2. Development of concepts toward the use of starter cultures 2.g. contribute to the development of characteristic properties such as taste. Through the ages. the initial phase of the fermentation process is shortened and the risk of fermentation failure reduced. The production of metabolites (e. Microorganisms. Enterobacteriaceae) may provide an additional advantage during fermentation. food fermentation dates back at least 6000 years. specifically for their adaptation to a substrate or raw material. Being adapted to the substrate. 1990). in substrates that are rich in fermentable sugars. Fermented foods can. Spontaneous fermentations typically result from the competitive activities of a variety of contaminating microorganisms. perhaps over thousands of years. mentation process. The majority of small-scale fermentations in developing countries and even some industrial processes such as sauerkraut fermentations are still conducted as spontaneous processes. eventually dominate the process. As a technology. which may possess features that are desirable for use as starter cultures. Fermented foods are treasured as major dietary constituents in numerous developing countries primarily because of their keeping quality under ambient conditions. Traditional approaches: spontaneous fermentations and back-slopping Modern starter cultures are selected either as single or multiple strains. shelf life and safety. Traditional fermentation process still serves as a substitute where refrigeration or other means are not available for the safekeeping of food.g. Repeated use of back-slopping results in selection of the best-adapted strains. starter cultures facilitate control over the initial phase of a fermentation process.
toxic components or residues. utensils and from the environment. 2002). applied. result in spoilage and/or the survival of pathogens. evaluation and control of hazards that are of significance for food safety (Amoa-Awua et al. typical of industrialised countries and used in various fields of food fermentation Foodstuff Sauerkraut Various vegetables Vegetable juices Soy products Sour dough Wine Dry sausage Dairy products Single-strain cultures + + + + + + + + Multiple-strain cultures À À À À + + + + Mixed-strain cultures À À À À + À À + Back-slopping +a À À À + À + (À) 199 À . Precautions should also be taken against the introduction or transfer of potential health hazards or factors that are potentially detrimental to quality during the fermentation process. Application of HACCP to fermentation is thoroughly covered elsewhere in this publication (Motarjemi and Asante. Inoculation with starter cultures does not provide an absolute guarantee against failure of fermentation processes. and on legume food substrates such as soya beans. traditional fermentations are reliant on moulds as the dominant organism. W. 3. for failure. In Southeast Asia. presents a scientific and systematic approach for enhancing the safety of foods. consumer expectations and technical requirements dictate to a large extent the nature of the starter culture to be used.or semisolid-state fermentations are widely accepted and appreciated by consumers in most African countries. through the identification. Hygiene. which differ across regions and continents. From a technical viewpoint. Selection of starter cultures and their application in small-scale fermentations 3. During this early phase which is associated with the lag phase of microbial growth. contaminating microorganisms on raw materials.2005-2007 For Evaluation Only. 1993. This implies the maintenance and control of technical parameters that ensure the desired outcome of the fermentation process. Approaches and considerations for the selection of pure cultures Considerations for applying starter cultures at the household level should take into account cultural traditions.1.4. nor does it eliminate health hazards associated with pathogens.Edited by Foxit Reader Copyright(C) by Foxit Software Company. mixed-strain culture. Metabolic activities of desirable fermentation microorganisms must be supported by observing the basic principles of Good Manufacturing Practice (GMP). however. Lactic fermented cereals produced by small-scale spontaneous solid. Beneficial attributes of the substrate. from primary production to final consumption. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Table 1 Starter cultures. not used. single-strain vs.e. dietary habits and raw materials. WHO. 1998. +. toxinogens. i. Source: Buckenhuskes.. on the other hand. logistical factors and the willingness of the small-scale processor to accept new approaches is critical in any assessment of the feasibility of introducing the use of starter cultures in small-scale fermentations. cost/benefit ratios. This phase can be shortened by inoculation either through back-slopping or with the use of selected starter cultures. Failure of fermentation processes can. The Hazard Analysis Critical Control Point system (HACCP). thereby creating unexpected health risks in food products. 2. which would otherwise be considered safe. In addi- .H. safety and quality considerations in support of HACCP approaches in small-scale fermentation processing Fermentation is generally considered as a safe and acceptable preservation technology for improving the hygienic quality and safety of foods. ¨ a Brine from a previous fermentation. 1995). slowly increase in number and compete for nutrients in order to produce metabolites.
Numerous reports indicate that Lactobacillus brevis. antimicrobial properties. and contribute more specifically to biological enrichment through the biosynthesis of vitamins and essential amino acids. 1998). The use of mycotoxin contaminated raw materials for fermentation in developing countries. there has been a considerable focus on the inclusion of mycotoxin-degrading strains in starter cultures. fermentation metabolites (e. (iv) Improved safety and reduced hygienic and toxicological risks. Westby et al. 3. reduced fermentation times. (vii) degradation of antinutritive factors.H. adaptation to a particular substrate. The probiotic properties of strains involved in food fermentations are also being studied in light of their potential contribution to the improvement of general health and well being. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 tion. lower risk if diarrhoea. improved process control. In recent times. 1994. 1997). back-slopping. homofermentation) and the ability of single or mixed strain cultures to produce desirable sensory qualities in the fermented product. such as reduction of costs (e. fermentum. The selection of suitable starter strains should take into account their interactions in mixed cultures. such as phytic acid and phenolic compounds. therefore. application of the HACCP system and education and training. visual appearance. 1994. Furthermore. include: (i) competitive behaviour. hetero. flavour and quality attributes and competitive growth behaviour in mixed cultures (Holzapfel. (vii) detoxification.. prior to their use in small-scale operations. The introduction of starter cultures should be considered within the context of realistic prospects for: information transfer minimal technical adjustments to small-scale ‘‘low-tech’’ food fermentations. the introduction of starter cultures in traditional small-scale fermentations should incorporate considerations for improving processing conditions and product quality through: (i) rapid accelerated metabolic activities (acidification or alcohol production). The rationale for such novel approaches is now discussed.2. 1997. Pedio- . Some LAB and yeast strains associated with fermented foods. reuteri.g. These include differences in growth rate. a minimum set of standards or quality parameters for the handling and maintenance of these cultures would need to be developed for use at the artisanal level.. are perceived.. texture.vs. L. 1997). aroma. Single-and mixed-strain cultures must. which vary even among strains. Ideally. (iv) the rate of acid or alcohol production. Technical considerations Technical aspects of starter culture development should incorporate considerations relevant to adoption of the starter to the substrate. and within the food substrate. (ii) improved and more predictable fermentation processes. According to Holzapfel (1997). Holzapfel et al. L. a multifunctional strain is targeted.g. Selection criteria for starter culture development Spontaneous food fermentations are neither predictable nor controllable. the rate of acid production. adaptation and the repeated use of specific utensils can contribute to the selection of microbial populations typical of a fermentation process. Smith et al. plantarum. L. (ii) antagonism against pathogens and spoilage microbes. viability and survival. improved safety attributes (e. therefore.g. to serve upgrade the nutritional value of foods.1. 3. Other factors. ability to degrade antinutritive factors. (viii) probiotic features (Holzapfel. consistency). are capable of degrading antinutritional factors. which should be considered. detoxification of cassava) and reduced preparation procedures for the final product.200 W. improved sensory quality (taste. reduced risk of spoilage (increased shelf-life). selected strains may enhance the general benefits of spontaneous fermentation such as improved protein digestibility and micronutrient bioavailability. poses a special challenge for the selection of strains that are capable of mycotoxin detoxification (Adegoke et al. Modern approaches incorporate considerations for technical safety and health-promoting features in the selection of the most optimal strain(s) for a process. Environmental conditions. be tested at the pilot scale.. The prospect of applying starter cultures will become attractive to the small-scale processor only if benefits. with consideration for the behaviour of these strains under defined conditions. (v) organoleptic changes. (iii) desirable sensory attributes. Pure cultures isolated from mixed populations of traditional fermented foods exhibit a diversity of metabolic activities. (vi) primary metabolites of fermentation.2. Incorporation of these organisms into starter cultures may. energy). Commercial starter cultures generally originate either from food substrates or from the processes in which they are applied.
palm wine and Asian ´ beverages. 1999) reported a stimulating effect of the yeast Candida krusei on L. Organic acids.g. however. moulds and yeasts Gram-negative bacteria Different bacteria Some LAB and Gram-positive bacteria.1. acidification to pH values of less than 4.. 1995. 1996. confirm that a number of metabolites. 1997. most traditional fermentations results from the combined metabolic activities of different types of microorganisms. such as L. Leuconostoc mesenteroides frequently dominates the early stages of most spontaneous fermentations. 1998) have been determined to be superior starter cultures for meat fermentations. Fermentations involving yeasts (alcoholic fermentations of beer and palm wines). Torula and Hansenula.2. inhibitory spectrum according to producer strain and bacteriocin type . Proteolytic enzymes present in food substrate are capable of inactivating bacteriocins.H. such as rice wines and Indonesian tape. 1997. resulting from metabolic activities of micro- organisms and their competitive interactions. Dominant microbes of these fermentations do not appear to be associated with any health risks. some yeasts and fungi Pathogens and spoilage organisms. natto (Japan) or kinema (Himalayas)] and LAB are generally recognised as safe (‘‘GRAS’’). fermentum and L. 1997. Bacteriocins.W. produced during the fermentation process. 3. L. exhibit antimicrobial properties which may contribute to the safety of lactic fermented foods (Table 2). Indeed. brevis during a mixed starter culture fermentation of the fermented maize ´ product. Candida. casei (paracasei) and other Lactobacillus spp. particular bacilli [alkaline fermentations e. mawe.2 constitutes a major safety concern in fermented foods. notably endospore-formers Gram-positive bacteria. while the initiation of milk fermentations is typically associated with Lactococcus lactis. strains of Saccharomyces cerevisiae eventually dominate most spontaneous alcoholic fermentations as in the production of African opaque beers. Oyewole. Lactic fermented foods in particular are considered to be safe and wholesome. 3. Bacteriocins are antimicrobial substances of a proteinaceous nature that are active against closely related bacteria.g. Although the growth rate of these yeasts is lower than that of bacteria.2. some fungi Putrefactive bacteria. especially in protein-rich foods Wide spectrum of bacteria. This is quite possibly the case for root crops. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 201 coccus pentosaceus and P. Main target organisms Putrefactive and Gram-negative bacteria. Holzapfel. followed by L. hydrogen peroxide and bacteriocins. clostridia. mesenteroides. soumbala (Burkina Faso). These beneficial microorganisms serve to some extent in safeguarding against pathogens and spoilage organisms. curvatus (Hammes and Hertel. On the other hand. Hounhouigan et al. Recent observations.2. (1994. Several LAB are associated with meat and fish fermentations. acidilactici exhibit superior performance in lactic fermented cereal and vegetable products (Steinkraus. Plant materials containing fermentable sugars provide suitable substrates for the yeast species Saccharomyces. They exhibit a narrow of activity but are not active against Gram-negative bacteria. Bacteriocins from LAB may be classified into three structural groupings on the basis of their physico-chemical and Table 2 Metabolic products of lactic acid bacteria which exhibit antimicrobial properties Product Organic acids Lactic acid Acetic acid Hydrogen peroxide Low-molecular metabolites Reuterin (3-OH-propionaldehyde) Diacetyl Fatty acids Bacteriocins Nisin Other Source: Holzapfel et al. as for dawadawa (Nigeria and Ghana). Lee. Antagonism This is the combined effect of different biological factors. 1997). such as acetic acid (from heterofermentative LAB).2. moulds (e. such as pathogens. which show strong antagonistic effects in the undissociated form at lower pH values. sakei and L. are particularly effective in inhibiting Gram-negative bacteria. tempe fermentations). during maturation.
1992) and may. 1981. Combined lactic and yeast fermentations have also been shown to improve the protein digestibility of cereal porridges (Graham et al. no recommended limitations for the intake of the L(+)-lactic acid isomer. 3. Leuconostoc spp. 1986. while a racemate (DL) is produced for L. Lorri.4.H. isoleucine.2. such as soak- .. indicating the importance of the length of the fermentation process (Holzapfel. Khetarpaul and Chauhan. 1987. These antinutritional factors. 1986.3. Nche. Lactic acid isomers produced by lactobacilli and pediococci are species specific. sakei. Bacillus cereus and Clostridium dificile. 1997). bacteriocinogenic LAB strains are of special interest in view of their possible application in food safety assurance. 1968). methionine and even tryptophane (Kazanas and Fields. WHO recommendations indicate a maximum daily intake of 100 mg/kg body weight of this nonphysiological lactic acid isomer (WHO. tryptophane and methionine deficiencies in cereal proteins contribute to malnutrition in developing countries (Holzapfel. 3. for example. 3. 1995). Lactic fermentation has been shown to lower the levels of proteinase inhibitors in cereal porridges thereby increasing the availability of essential amino acids. Enterococcus and Carnobacterium produce > 90% of the L(+)isomer as an end product of sugar fermentation. contain a number of antinutritive fac- tors. 1995). mesenteroides 92 activity showed that a significant decrease in trypsin inhibitor activity was affected only during the stationary phase of growth. however.4. Proteinase inhibitors. the chelating properties of phytic acid may significantly reduce the bioavailability of minerals. 106 (Table 3). A kinetic study of L. leucine. such as cereal-based diets. 1994). examples of which include Streptococcus.. The lactic acid isomer The lactic acid isomer produced during fermentation is typically related to the LAB species from which it is produced. The nature of the lactic isomer is of concern. Mbugua et al. delbrueckii (all subspecies) on the other hand produce D( À )-lactic acid. since high levels of the D( À )-lactic acid isomer are not hydrolysed by LDH enzymes in humans and are. therefore. Mbugua. such as lysine. 1992). 1995. and L. magnesium and zinc. Furthermore. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 antimicrobial properties (Schillinger et al. Phytic acid and tannins are antinutritive components typical of cereal and legume foods. by an individual having a 50 kg body weight. capable of causing acidosis. The L(+)-isomer is produced by L. such as calcium. such as Listeria monocytogenes. 1997). however. coupled with the lysine. casei.. These compounds are of concern since they may reduce both iron and mineral bioavailability in cereal and legume-based diets. Though relatively uncommon in fermented foods (Olasupo et al. It is effective in reducing proteinase inhibitors (e. Essential steps in traditional household-level processing. LAB genera. as reported for a number of foods of plant origin (Chavan and Kadam. 1993. Protease and amylase inhibitors..2. Bacteriocinogenic LAB have been shown to effectively inhibit the growth of pathogens.. An approximately 50% reduction in trypsin inhibitor activity was observed in our laboratories for L. serve to improve the protein quality of cereal grains. Fermentation may serve to improve the nutritional value of cereal staples through the reduction of antinutritive factors. sorghum and millet) which are often admixed with legumes in order to upgrade their protein content. thus. iron. therefore. L(+)-lactic acid producing strains should. There are. even under in situ conditions (Holzapfel et al. LAB strains. 1995). Consumption of 1 l of a fermented gruel containing 1% of DL-lactic acid. Holzapfel et al.2. 1989). isolated from Ghanaian fermented foods..202 W. Mbugua et al.g. Staphylococcus aureus. Phytic acid and tannins.2. trypsin inhibitor) in legumes and tannins. could potentially result in the intake of the maximum recommended levels of this nonphysiological acid. Antinutritive factors Antinutritive components are of particular significance in unbalanced diets. 1993.4.2. Lactococcus. Cereal staples (maize.. all heterofermentative lactobacilli and practically all Weissella spp. polyphenols (from millets and sorghum) and lectin-related haemagglutinin activities in legumes and tannins.. Lorri. adversely affect the protein and starch availability of these foods. 3. plantarum strain 91 and Leuconostoc sp.1. and disulphide cross linkages in sorghum prolamine proteins (Hamaker et al. 1989. differ in their ability to degrade trypsin inhibitor under defined conditions. be preferentially selected for the fermentation of beverages.
(1974) with synthetic benzoyl DL-arginine-p-nitro anilide as substrate (Holzapfel. Soaking (Ogun et al. whilst it appears to be a constitutive property for L. plantarum 91 L. Phytase activity is not detectable for Bacillus spp. 1997). L. pearl millet (Mahajan and Chauhan.6 53.8 203 a Investigations were conducted in a synthetic liquid medium containing 5 mg TI/ml. buchneri.2 26. 1997). and cause flatulence. L.. 62 Reduction of TI (mg) 2. 1989). A comparison of the effects of spontaneous fermentation. 1986). Khetarpaul and Chauhan. Extensive studies using both pure and mixed cultures have shown that neither sucrose nor raffinose is utilised by the tempe mould Rhizopus oligosporus (Sorensen and Hesseltine.41 1. capable of degrading phytic acid on incubation at 37 jC for 120 h (Holzapfel. 1990) were determined to be important processing steps for reducing the oligosaccharide content of legumes. 2000) revealed that all three types of fermentations contributed significantly to the detoxification of cassava. dextranicum and Weissella paramesenteroides. may cause severe intoxications following the consumption of raw or unprocessed bitter cassava (Holzapfel.. 1996.08 2. 1983). mesenteroides and ssp. mesenteroides ssp. acidilactici and P. 1993). a fermented cereal – legume product (Reddy et al.2.. appears to be variable (Milliere et al.. 1966) although Shallenberger et al. such as L.. Degradation or inactivation of natural toxins The degradation or inactivation of toxins by pure cultures during fermentation has received considerable attention in recent times.65 1. 106 Lactobacillus sp. associated with the fermentation of the African locust bean Parkia biglobosa which is used in the preparation of iru or dawadawa (soumbala) (Aderibigbe and Odunfa. (Ejiofor and Okafor. maize (Lopez et al. however.8 21. Naturally occurring toxins. 1995) and yeasts and moulds (Hahn. Incubations were conducted at 30 jC for 5 days.34 Percent reduction 48. Raffinose. fermentum. non-tannin containing cereals (Svanberg et al..86 1. Oligosaccharides. Even with strict regulations on maximum tolerable levels. 1994). Essers et al. 1981. Bacillus spp. germination and lactic fermentation. L.. control ing. plantarum strains isolated from fermented Ghanaian maize products were able to ferment raffinose.W. back-slopping and the use of starter cultures for the reduction of cyanogenic glucosides in cassava (Kimaryo et al. The production of a-galactosidase by LAB species. 1997). 1989) and germination (Abudu and Akinyele. phytic acid degrading ability is relatively rare among pure LAB cultures. although endogenous linamarinase enzymes present in cassava play a significant role in the process. Detoxification during the fermentation of cassava is brought about primarily by microbial activity (Westby and Choo. 1989) and idli.0 37.6 13. 3.. fermentum 103 Pediococcus sp. salivarius (Mital et al. L. 3. 1990. Mycotoxins Mycotoxins. stachyose and verbascose are oligosaccharides that typically occur in legumes and cereals. The TI concentration was determined according to Kakade et al. 1995.89 1. which are raw typical materials for traditional fermented foods in most African countries (Holzapfel. 1991). Lactobacillus spp. may contribute to a reduction of these inhibitors. 1988).5. 1997)..0 24. Essers et al. 1990). Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Table 3 Degradation of trypsin inhibitor (TI) by lactic acid bacteria isolated from aflata in Ghanaa LAB isolate L. cellobiosus and L. These sugars possess a-Dgalactosidic bonds which are resistant to cooking and small-scale processing.. Amoa-Awua and Jakobsen. 17 Lactobacillus sp. plantarum strains are.22 0.2.4. plantarum strains giving the best results. in particular aflatoxins and fumonisins pose a major risk in stored cereals. Some L. 1989.. 41 Laactobacillus sp.3. but which can be hydrolysed by a-galactosidases produced by a number of moulds and by bacteria associated both with the digestive tract and with fermented foods. while strains of P.. 90 Pediococcus sp.2. diarrhoea and indigestion in humans. 19 Leuconostoc sp. (1967) determined sta- . with a starter culture consisting of L. 3.68 0. Soaking has been shown to activate endogenous phytases in most cereals and legumes.H. Trugo et al.4 17. brevis.6. Olasupo et al. such as the cyanogenic glucosides (linamarin and lotaustralin) in cassava. 1987. Although lactic fermentation has also been shown to reduce the phytate content of white sorghum (Svanberg and Sandberg. 1997). 1995) play an important role in cassava processing. 1973) and is probably inducible in L. (Amoa-Awua et al. chyose to be relatively slowly hydrolysed. plantarum (ATCC ´ 8014) (Ahrne and Molin. pentosaceus were unable to do so (Table 4).
1997). Nos. exhibit the potential for degrading histamine and tyramine through the production of mono. while Van Veen et al. Steinkraus (1983). been reported (Nout et al. some authentic LAB strains and others isolated from fermented Turkish foods (L. 3. 1 – 21. 21. 70. Inocula consisting of a portion of a fermenting substrate may be preserved by dehydration (air. Incubation was conducted at 30 jC for 3 days (Holzapfel. Studies conducted under defined conditions using single LAB strains isolated from Ghanaian kenkey (aflata) resulted in reduced production of Alternaria toxin (Holzapfel. 91: from Agbelima. a member of the Gram-positive phylogenetic group of the Actinomycetales (Holzapfel et al. which are adapted to the substrate. 31 – 47: from fermenting maize/white cowpeas mixture (70:30). 39.and di-amino-oxidases (Leuschner et al. ¨ Certain LAB. 53 – 70: from fermenting maize/red cowpeas mixture (70:30). putrescine.. 100: from Aflata (for Ga-Kenkey) after fermentation. Nos. 3. buchneri. 68 90 100 92 DSM 20343T Acid production ++ + À À À À ++ Acid production: À = negative.2.H. 38.004% chlorophenol red as indicator. such as the porous material of a gourd. 1992). 60. 46. No. thus. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Table 4 Raffinose fermentation by selected LAB strains isolated from fermented maize products of Ghana Species Lactobacillus plantarum Lactobacillus plantarum Lactobacillus plantarum Pediococcus pentosaceus Pediococcus acidilactici Leuconostoc mesenteriodes ssp. 1994. A number of bacteria associated with these fermentations. mechanisms for mycotoxins in developing countries are inadequate. although still controversial. 8. Natural preservation of microorganisms can also be accomplished with the use of a carrier. + = weak. Neurospora and the tempe mould. unpublished data). 1997). indicate that some mycotoxins may be degraded or inactivated during cereal fermentations. however. 31. a Origin of strains. and can neither be applied to agricultural products sold in rural markets. Buckenhuskes et al.a 1. In addition. oligosporus. R.7. 69 37. Qualitative fermentation tests were performed in MRS broth (pH 6. 92: from fermenting maize (Aflata) during Kenkey production. 7.. 43. 1998). such as L. during fermentation. Nos. 44. No.204 W. in fermented products of plant and animal origin. an organism which appears to be wrongly classified and which has now been identified as Nocardia corynebacterioides. provided the product is maintained in the dehydrated state. 64. + + = strong. In traditional back-slopping.. reported reduced aflatoxin B1 (AFB1) levels during Indonesian ontjom fermentations.. after cooking. Experience with the application of starter cultures in small-scale operations Experience gained in the field of traditional fermentation technologies has shown that the addition of malted grains to fermentation media increases the rate of fermentation due to the endogenous amylolytic activity of the grains. plantarum and L. however. 1997). inoculum from a previous batch of fermented dough contains large numbers of desirable microorganisms in an active state. Dehydration enhances the viability of microorganisms over relatively long periods..4) containing 1% raffinose (instead of glucose) and 0. fermen- . Numerous reports. Biological detoxification of AFB1 through degradation has. 65. Biogenic amines Biogenic amines are frequently produced by amino acid decarboxylase positive microorganisms. 53. tyramine and cadaverine. 1994. far only been proven for Flavobacterium aurantiacum (Line et al. 90: from Yakeyake after fermentation. Fermentation processes may also be accelerated through the addition of a starter obtained from a previous fermentation batch (backslopping).or sundrying) and grinding into a powder. 1998). No. 55. Mesenteroides Strain nos.3. D’Souza and Brackett. The occurrence of biogenic amines in traditional fermented foods has. nor to those used at the household or small-scale level. have been shown to produce biogenic amines. (1968) observed that the aflatoxin content of peanut press cake was reduced by both the ontjom mould. such as histamine. 91 58. 47. pentosus) were observed to reduce patulin concentrations by >60% in semisynthetic medium (Arici.
L. large-scale industrial applications. L. single. Hansenula spp.. acidophilus ‘‘thermophilic’’ LAB L.4. yeasts (Saccharomyces spp. camel milk and wheat sheep milk and wheat 2. dried kishk Trahanas Addition on a daily basis back-slopping commercial cultures Kefir Russia (Caucasus) goat milk. Turkey cow milk. These starters contain mixed cultures of filamentous fungi (e. plantarum. ¨ bulgaricus. Mucor. Interesting examples of mixed-culture dough inocula prepared either in the form of dried powders. cow milk 25 – 30 g of kefir grains per 500 ml milk kefir grains refrigeration . are found in several Asian countries where they are used for the inoculation of starchy substrates in the production of alcoholic beverages. Actinomucor). L. they have not been adequately studied. bacilli S. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 205 tation utensils or an ‘‘inoculation belt. (ii) flexibility and simplicity of maintenance and handling. Amylomyces. S. L. (v) handling and storage at the household level.0% 1/3 (w/w) back-slopping Laban zeer. fermentum yeasts.H. Product groups associated with traditional inoculation methodologies are summarised in Tables 5– 8.vs. sojabeans cow milk. L. (iv) job creation and income generation in rural areas. delbruckii ssp. 5 – 10% (winter) Storage/starter application lyophilised back-slopping Microorganisms Strains of one or more of: Lactococci.W. Although such preservation methodologies are common to many regions and probably have a long tradition. thermophilus. (iii) minimal losses due to fermentation failure. delbruckii ssp. Iraq. Inoculations with a single-strain culture can eventually result in a mixed-strain fermenta- Table 5 Starter cultures used for traditional dairy products Product Dahi Country India and neighbour countries Raw materials buffalo milk. inexpensive utensils that are readily available. determines dominance of the best adapted strains.’’ such as that used in Ghana for the initiation of pito beer fermentations. These old traditions in starter preparation. and are referred to by different names in accordance with the location of production.) and LAB (species of Lactobacillus and Pediococcus) (Tamang. ¨ bulgaricus or L. and a number of attractive challenges and benefits to the entrepreneur: (i) the use of simple. L. North Africa Greece. thermophilus and L. sheep milk. brevis. casei. where processing conditions and continued recycling of a portion of a previous batch.5 – 3. mixed-strain starters Spontaneous fermentations typically result from the competitive activities of different microorganisms. flat cakes or hard balls. Pichia spp. 3. Rhizopus. preservation and distribution present an extremely valuables basis for the development and application of other types of starters in small-scale processing. (vi) distribution and sale in local markets. The complexity and variability of microbial populations associated with these fermentations is somewhat reduced in back-slopping operations.. cow milk Amount of inoculum 1 – 2% (summer). L. Cyprus. Small-scale vs. kefiranofaciens Tairu Kishk Kuschuk Malaysia Egypt.g. brevis. 1998). cremoris. Strains best adapted and with the highest growth rate dominant during particular stages of the process.
bacteria A majority of these products are manufactured by ‘‘spontaneous’’ fermentation. Sri Lanka Raw materials rice. cerevisiae toddy: mixed culture years/LAB yeasts. a Lactic acid bacteria. dehydration Microorganisms L. Sudan tef (Ethiopia). cerevisiae. spontaneous mutation or through the loss of key physiological properties (e.H. however. a Lactic acid bacteria. tion if raw materials are not sterilised prior to inoculation and maintained axenic (free from foreign microorganisms) throughout strict process control. Catso wheat.and acid-alcoholic fermented gruels Product Mawe (sourdough) Mahewu Country Benin Raw materials Maize Inoculum (starter) previous batch small portion of wholewheat flour fermenting kocho ‘‘Inoculation belt’’ Storage conditions active fermentation (?) Microorganisms heterofermented lactobacilli and yeasts mainly heterofermented lactobacilli (yeasts) LABa yeasts Lactobacilli. Torulopsis Puto Philippines Injera (Ethiopia). soybeans rice Inoculum (starter) buttermilk. Examples given refer to alternative options. relatively easily degraded by bacteriophage infection. S. yeasts Southern Africa Maize Kocho (a flour) Pito (traditional beers) Ethiopia Ghana. peas. black gram. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Table 6 Starter cultures applied in the preparation of traditional acid-leavened cereal and legume products Product Idli (Dosa) Country South India. mesenteroides.g. Examples given refer to alternative options. faecalis. commercial yeast. cowpeas. Deterioration in culture performance Table 7 Mixed starter cultures applied in the production of traditional acid. cerevisiae Candida and other yeast spp. faecalis. acetic acid. (b) powdered puto irsho (ersho) and fermentation container (bohicka) baker’s yeast or toddy (fermented drink) vigorously fermenting dough (a) neutralisation of ground slurry. Single-strain cultures offer advantages of improving both process control and the predictability of me- tabolic activities within the culture. Anjeira (Sudan) Ethiopia. LAB. . E. S. (b) dehydration cool place in home L. plasmid-mediated fermentation of lactose). west Africa ensete (false banana) Sorghum (maize millet) pit (fermentation) drying Most of these products are still manufactured by ‘‘spontaneous’’ fermentation. maize.206 W. sugar). They are. dried idli Storage conditions refrigeration. sorghum (Sudan) or other cereals rice or wheat flour Hopper (Appa) Sri Lanka (a) ‘‘leba dura’’ (ground slurry/ 18 h. mesenteroides. E. LABa Kisra Sudan sorghum active fermentation S.
Variation in product quality with the use of mixed strain cultures can be minimised through proper process control. 1993). such as in the production of African opaque beers. In large-scale fermentations. better suited to most smallscale operations. The association of LAB with the human environment and their beneficial interactions. Mixed strain cultures. consistent end product quality is achieved over extended time periods through the use of defined single-strain cultures and properly controlled processes. Tamang (1998) and Merican and Quee-Lan (1989). in particular Saccharomyces spp. The largest spectrum and richest variety of lactic fermented foods is probably found in Africa. Hansenula and others. LAB are major importance among bacteria associated with traditional fermented foods. handling and application of pure singlestrain cultures and for strict process control at all stages of the fermentation. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Table 8 Ragi-type starter cultures Product Tape ketan Country Indonesia (JAVA) Himalayan regions (India. on the other hand. combined with the long tradition of lactic fermented foods in many cultures. are less susceptible to deterioration and are. due to one or more of these effects adversely affects the fermentation process. such as rice wines.H. are typically associated with spontaneous alcoholic fermentations. they contribute to a more complex sensory quality. both in food and in the human intestinal tract. on the other hand. are not available or attainable in most small-scale operations. thus. Bhutan) Thailand China. Plant materials containing fermentable sugars provide suitable substrates for yeast species of Saccharomyces. In Europe. is readily available on the market throughout Africa. Although moulds play a minor role in the fermentation of foods in Africa. chrysogenum) (Geisen. Ahab Krachae Lao-Chao Tapai perlert Rice wine Tapai ubi tape kerccella (bran) rice millet rice (millet) rice rice Baseam Loogpang Chin-yueh ragi tapai ragi samsu Ragi Sources: Steinkraus (1996). storage and applications. Several factors must be taken into consideration when evaluating the use of LAB as starters . traditional mould-ripened foods are mainly restricted to bluemould (Penicillium roqueforti) and white-mould (P. camemberti) cheeses and mould-ripened fermented sausages (containing either P. Dehydrated yeast.. Candida. such as those of the ragi type. Nepal. other cereals Marcha. yeasts and LAB Jaanr Chiang rice millet. It is also applied in small-scale beer brewing (Tables 6 and 7). Taiwan Nalyoia Malaysia Indonesia Raw materials rice Inoculum (starter) Ragi Storage conditions Dehydrated (air. have led to the conclusion that these foods may be ‘‘generally recognised as safe’’ (‘‘GRAS’’). they are of major importance in Asian food fermentations. such as the degradation of undesirable factors.W. ´ palm wines and Indonesian tape. Torula. Mixed strain cultures are relatively unaffected by fluctuating conditions of handling. Selected strains of S.or sundried) 207 Microorganisms different moulds. In addition. whilst producing favourable synergistic effects. Bakhar. nalgiovense or P. Modern equipment for the preparation. which is mainly applied in bread making. cerevisiae are used for the industrial production of both western style and traditional African beers. Spontaneous alcoholic fermentation of palm wines and most opaque cereal beers. flavour production and accelerated ripening and maturation. palm wine and Asian types of beverages. These yeasts.
should be no absolute reason to disqualify the use of food grade strains of these and other LAB species from their potential use in food fermentations and even as probiotics. (i) The traditional starter kudeme is used as an inoculant in West Africa. 1997. results in large numbers of Mucor and Rhizopus spp. Microbial growth takes place over a 2– 5-day period under ambient conditions. (ii) Lactobacillus (both homo. Leuconostoc and. to a lesser extent. widespread in that region. during which gradual desiccation of the rice balls occurs. The use of back-slopping approaches for inoculation are. (v) Suitable cultures for fermentation must be selected at the strain level since not all strain of a species are equally suitable for use as starters. E. Bakers yeast is used worldwide in bread baking. species of the genus Streptococcus are generally regarded as pathogens. suggest sufficient potential for the use of LAB starters in small-scale food fermentations in Africa (Holzapfel. Iraq) and North Africa dried kishk or laban beer is used as an inoculum for kishk and kuschuk production (Table 5). (i) Not all LAB are of equal technical and practical importance in food fermentations. the production of sauerkraut and dill cucumbers) are spontaneous although technically well controlled. rhamnosus. 1989). The association of certain strains of Enterococcus faecium. (vi) A number of industrial lactic food fermentations (e. Studies into the application of selected LAB strains for traditional fermentations. In some countries of the Near East (Egypt. preservation and application of starter cultures Perhaps the oldest traditions in the preparation. distribution over extensive areas. 1998).g. which consists of flax of hennep. typical of Ghana and some countries in West Africa.. Lactococcus. Powdered ragi from a previous batch is sprinkled as an inoculum over the paste prepared from rice flour and water and moulded into a ball. (iii) The genus Bifidobacterium. 1997). ragi formulations are maintained proprietary by manufacturers. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 (Holzapfel. Slow drying of ragi balls during the rainy season.. The inert surface of the belt or woven rope. 1999).H. Holzapfel et al. poses a great challenge to both the food microbiologist and the potential entrepreneur. however. It is also applied in brewing and the production of wine at the household level. is often grouped as part of the LAB for its probiotic functions (Reddy and Rivenson. 1998) (Table 8). Salminen et al. 1989). Relatively little information is available on starter culture traditions in Sub-Saharan Africa. Sundrying may destroy some microorganisms and thereby reduce viable numbers. while slow and insufficient airdrying during the rainy season may result in contamination and poor quality starters. Handling. with exceptional cases of endocarditis. One example of a preserved starter is the inoculation belt. LAB starter cultures are not yet commercially available for the small-scale fermentation of traditional African foods. Inoculated balls are placed on bamboo trays and either covered with muslin cloth (Malaysia) or with ferns (Himalayas). and sophisticated methods for propagation and preservation are factors which complicate LAB starter culture development.1. (iv) With the exception of S.and heterofermentative). Bakers yeast is commonly used in the fermentation of sorghum and other cereal beers in Africa (Holzapfel. 1993. Although ragi production does not incorporate the use of specialised equipment. for preparing the fermenting cassava dough. agbelima (Amoa-Awua and Ja- .208 W. 1997). faecalis and L. Low expected turnover. 1996. Tamang. maintenance and distribution of starter cultures for small-scale fermentations 4. This is particularly true for the mixed-culture dough inocula. The predominance of lactic food fermentations in Africa and the contribution of these fermentations to food safety deserve special attention. Pediococcus. nor are all equally well adapted to a food substrate. (Merican and Quee-Lan. such as the ragi-type starter cultures which have been used for centuries in the production of a variety of sweet and sour alcoholic beverages and pastes (Steinkraus. however. The shelf life of dehydrated starters may be enhanced by storage in an airtight container. Traditions in the conventional handling. 4. Enterococcus and Weissella are the genera which generally occur in traditional fermented foods. thermophilus. Making them available to the small-scale processor. however. facilitates the preservation of essential microorganisms during drying and storage. handling and distribution of starter cultures are to be found in the different regions of Asia (Lee and Fujio. although phylogenetically not related to LAB.
pragmatic approaches and economic considerations Apart from experience with the traditional use of mixed culture inoculants of the ragi type in Asia. was shown to enhance the viability of LAB strains (Nche et al. kenkey. 1994). Selected strains may be improved through the application of genetic technologies. such as gene disruption (Geisen and .W.. Kivunde is typically formed into small balls. (iv) Selection of microorganisms with desirable properties. Undesirable properties. health-promoting properties. These starter cultures may find application and might serve to improve small-scale fermentations even in rural areas. Recombinant DNA technology may be applied in the production of tailor-made starter cultures which would meet technical and metabolic requirements necessary for a specific fermentation (e. plantarum. Four major focal areas for research on starter cultures were recommended by WHO and FAO (FAO/WHO. This is not however the case in most rural areas of developing countries.. aflata applied in the preparation of the fermented maize-meal product. (ii) A stable LAB-enriched starter dough. Nche et al. 1989. a traditional product of the Western and North-Western Regions of Tanzania produced safe cyanide levels < 10 mg/kg during cassava fermentations (Kimaryo et al. 4. 1996). (ii) Establishment of an appropriate level of starter culture technology. Multifunctional considerations On the basis of all of the foregoing discussion. and feasibility of. 5. 5. overproduction of bacteriocins or of particular enzymes necessary for degradation of undesirable factors). nutritional value and even health-promoting properties of fermented foods by multifunctional starter cultures. Modern selection techniques (Zhong et al. isolated from kivunde. thereby indicating the potential for its extended storage and distribution as a starter.g. by refrigeration) of starters on a continuous basis is generally available in urban areas. however. Prospects for improving the safety. (iv) fermenting L. 2000). 1994). however. Approaches toward starter cultures with improved properties 5. such as yeasts and moulds. effective in inhibiting undesirable microbes. only be successful if the basic principles of good processing practices (GMP) are observed. distribution and storage (e. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 209 kobsen. such as mycotoxin or antibiotic production by food-grade moulds. it is clear that the selection of starter cultures should take account of properties beyond those of acid (by LAB) or alcohol production (by yeasts). Genetic improvements: pro and contra It is doubtful whether the most modern techniques and selection procedures would result in a multifunctional strain having all desirable metabolic features. accelerated acid production. have become a reality in our time. Research priorities for starter culture development were extensively reviewed elsewhere in this publication (Motarjemi and Asante. improved wholesomeness. Cabinet and drum-drying of this dough from a 54% to a 10% moisture content.g.H.. (iii) Development of appropriate starter culture delivery mechanisms. (3 –5 cm in diameter) and air-dried. It is not. 2002). required. may be eliminated by techniques. 1998) and the application of molecular biological tools have been covered elsewhere in this publication (Valyasevi and Rolle. (iii) Addition of CaCO3 (‘‘chalk’’) to fermenting substrates increases retention of the metabolic activities of LAB.. Logistical requirements. produces accelerated acidification and contains a natural selection of acid resistant strains (Nout et al. (i) Assessment of the need for. Infrastructure required for the manufacture. relatively little is known about the economics and practical constraints of starter culture supply and distribution to small-scale processors in developing countries. thereby preserving viable strains over extended periods. sensory characteristics.2. Information on the logistics of starter culture distribution in developing countries is.2. therefore. Such approaches will.1. CaCO3 confers this protective effect primarily through the neutralisation of lactic acid. 1996). upon identification and selection of suitable strains. These tools and techniques provide improved means for obtaining the most suitable microbial strains for each specific substrate and situation and have opened up opportunities for the development of ‘‘tailor-made’’ starter cultures. shelf life. using starter cultures. 2002)..
In addition. trypsin inhibitors and nutrient content of cowpea milk. substraterelated interactions and metabolic activities of different microbial groups.E. Int. approaches for strain selection and toxicological studies on possible degradation products. 1994. with the aim of reducing levels of biogenic amines in selected fermented foods. 1996. E. Appl. Growth and extracellular enzyme production by strains of Bacillus species isolated from fermenting African locust bean. A number of aspects of relevance to starter culture production should. The Third Biennial Seminar on African Fermented Food. (Eds. on key enzymes and on the role of technical and other process parameters. Iru. WAITRO. A large number of such optimised cultures already exist. 1995. S.... 1990. pp. Studies on microbial dynamics.O.g. 79.O. e. 1991. M. therefore. Jakobsen. E. (vi) Amino acid decarboxylase activ- ity as a negative selection feature for potential starter cultures.0267 and TS3 * CT-940344). (vii) Potential for the fermentative detoxification of mycotoxins. Antonie Van Leeuwenhoek 60. S. Bacteriol. I. The introduction of appropriate starter culture techniques may constitute one major step towards improved safety.g. Odunfa. Ghana. and studies on growth behaviour and technical performance of probiotic strains. These are gratefully acknowledged. Adegoke. M. Food Chem. small-scale and household level fermentation processes.. W. 6. development of in vitro selection methods for probiotic strains. quality and security of traditional small-scale fermentation.H. Lactic acid fermentation of cassava dough into agbelima.K. have provided a firm basis for improvement of traditional. Spontaneous mutations changing the raffinose metabolism of Lactobacillus plantarum. and mono-amino-oxidase activities as a positive selection criterion.Y.. July 1996. 69. and may serve as model for application in other regions. heat and processing time on the reduction of aflatoxin B.. Amoa-Awua.. References Abudu. 31. S. 45.. Denmark. Amoa-Awua. and the relevance of D( À )-lactic acid producing LAB strains in foods typically consumed in large quantities. Otumu. by synergistic effects among different antimicrobial agents and physico-chemical factors related to the food substrate. Taastrup.. Agriculture and Forestries (BMVEL) and the European Commission (STD projects TS2. The effect of germination on the oligosaccharides. A. Akanni. Traditional Fermented Food Processing.. levels in tuwo and ogi: two cereal-based products. M. . 1996. (v) Growth patterns. 161 – 166. W. M. aureus) and improvement of inhibitory action. J. receive special attention..O. Akinyele. (i) Information on inhibition kinetics of food-borne pathogens by typical LAB cultures under practical. 1990). Jakobsen. Food Microbiol. 87 – 98. (ii) Viability and survival of sublethally injured enteropathogens in fermented foods and their potential pathogenicity.). traditional beer types).. G. 87 – 93. the average daily intake of such beverages.J.. (iii) The role of bacteriocin producing LAB strains as an additional safety factor against Gram-positive pathogens (e. Nutr. Regulatory issues however preclude their use. product-specific conditions. The role of Bacillus species in the fermentation of cassava. As examples. stability and acidification potential of L(+)-lactate producing strains during smallscale operations. (iv) information on the typical concentrations of D( À )-lactic acid in traditional fermented gruels and beverages (e.. F. Appoh. the following should be mentioned. ISBN 87-87047-23-3. 35. Conclusions Knowledge on traditional fermentations is rapidly increasing. J. Plant Foods Hum. Aderibigbe. Acknowledgements Some data presented have been generated from research projects that were financially supported by the German Ministry of Nutrition. 7 – 15. ´ Ahrne. Jakobsen. 662 – 671.. M. 250 – 256.210 W. and in fact deserve the highest priority. In: Halm. Bacteriol.. Amoa-Awua.K. I. 1996. Artisanal level starter culture traditions in Asia have proven feasible over generations. W. J. an understanding and application of HACCP principles and the observance of GMP are of vital importance.A.A.g. Appl. Influence of grain quality. (viii) Studies on functional (probiotic) properties of LAB strains involved in traditional fermented foods.. 113 – 117. Molin. Focused studies toward the introduction of starter cultures for small-scale fermentations seem more than justified. Jakobsen. The role of microorganisms in the fermentation of agbelima cassava dough. G. Holzapfel / International Journal of Food Microbiology 75 (2002) 197–212 Holzapfel. 1990. Hammes and Vogel.K.
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