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Patience Mensah B. S. Drasan T. J. Harrison and A. M. Tomkins
The high incidence of diarrhoeal morbidity a' the onset of weaning is due in part to consumption of contaminated food. This paper discusses the possible role of fermentation as a household food preparation technology in the improvement of the microbial quality of weaning foods as well as in providing adequate nutrients for infant growth and development. It discusses the extent to which fermented foods provide adequate nutrients; the degree to which fermentation can reduce the levels of aflatoxins, hydrocyanic acid, and other toxins in foods; whether fermentation reduces contamination of weaning foods by pathogens; and the role of fermented foods in reducing diarrhoeal morbidity, severity, and duration.
The increase in diarrhoeal morbidity at the transition between exclusive breast-feeding and a mixed diet was presented as an epidemiological entity, "weanling diarrhoea," in 1963 . Contaminated food is one of the routes of transmission of diarrhoeal pathogens . Samples of food consumed by 70 children 518 months of age in Bangladesh showed that the proportion of food samples that contained Escherichia cold was significantly related to the child's annual incidence of diarrhoea due to enterotoxigenic E. cold (ETEC).
The precise extent of food-borne diarrhoeal diseases in young children is not documented, but a review by Esrey and Feachem  concluded that indirect evidence suggested that 15% to 70% of all diarrhoeal episodes may be associated with practices of food preparation, handling, and storage as well as feeding methods. Hands, water, utensils, feeding bowls, raw ingredients, and the surrounding environment are potential sources of pathogens in infant food. In areas where there is no organized sewage disposal, weaning-food contamination is magnified.
There is a wealth of evidence demonstrating the high levels of faecal contamination in weaning foods from developing countries [2; 4-9]. That foods especially prepared for feeding young children may become more contaminated than the foods consumed by the whole family is a matter of great concern . The problem is aggravated when infant food has to be stored at high ambient temperatures because of the lack of refrigeration. The heavy workload of mothers and lack of regular supplies of food, water, and fuel may prevent the preparation of fresh food for each meal during the day. All these are factors that together allow multiplication of enteropathogens to unacceptable levels.
A study from Peru  reported that, after one hour of storage, faecal bacteria increased threefold in weaning cereals and purées prepared from rice, maize, potatoes, wheat, and bananas. Studies from Bangladesh , India . Kenya , and the Gambia  have also shown evidence of multiplication of bacteria during storage. Against this background mothers are often advised to breast-feed for as long as possible in order to reduce the risk of diarrhoea from the consumption of contaminated food.
Although continued breast-feeding does play a role in the protection of children from diarrhoeal illness, such children stand a risk of malnutrition as breast milk becomes inadequate for growth [12; 13]. The need to weigh the relative risks of initiating and delaying weaning has been called "the weanling's dilemma" [9; 14]. Waterlow called it "the suckling's dilemma" , perhaps to emphasize the importance of continued breast-feeding after the introduction of semisolid food. These reports emphasize the need for weaning foods that are (1) appropriately timed, (2) nutritionally adequate, and (3) hygienically prepared. The question of appropriate timing of the first introduction of a weaning diet was critically reviewed by [Underwood and Hofvander . who emphasized the importance of achieving a balance between adequate nutritional intake and the risk of intestinal infection from contaminated food. In addition, the known interaction between infection and nutrition places added emphasis on the importance of weaning foods with little or no contamination in reducing diarrhoeal morbidity .
To make progress in addressing this public health problem of global importance, it seems clear that effective strategies are required in order to improve weaning food both hygienically and nutritionally. To achieve this goal, an emphasis on obtaining locally available foods that are hygienic as well as nutritious to supplement diets of breast-fed children in developing countries appears appropriate [14; 18]. This paper explores the potential role of fermentation in the production of nutritionally adequate and microbiologically safer weaning foods.
Fermentation - an overview
Fermentation is one of the oldest methods of preparing and preserving food. Fresh milk was fermented to produce yoghurt and cheese during the days of the Pharaohs . Vegetables were preserved by fermentation as early as the building of the Great Wall in the third century B.C. . A wide variety of substrates are fermented, including meat and fish, but the products of great relevance in young-child feeding are produced by the fermentation of cereals and pulses from Africa and Asia.
TABLE 1. Some examples of fermented foods from developing countries
|Food||Substrate||Cooked food type||Consumption|
|koko or akasa||maize||porridge||all ages|
|Kenya, Uganda, and Tanganyika||uji||maize, sorghum, and millet||porridge||all ages|
|India||indli||black gram and rice||porridge||all ages|
|Indonesia||tempeh||soy beans||porridge||all ages|
Sources: Refs. 21-29.
Recipes for the preparation of fermented foods are varied and may depend on the staple, the geographical area, and cultural preferences. For example. the preparation of porridge from fermented maize dough is carried out by one of three methods:
1. Winnowed grain is soaked in water at ambient temperature for one or two days, after which the water is drained before wet-milling. Water is added to the resulting meal to produce a stiff dough, which is then allowed to ferment spontaneously, and porridge is cooked from this dough. The fermented maize dough porridge called akasa in Ghana is prepared by this method .
2. The second method, which is employed in the preparation of Nigerian ogi, involves preliminary preparation of maize meal as described in method 1. The meal is strained to remove all chaff after the addition of a large volume of water, thus giving a smooth-textured product. The mixture is allowed to ferment overnight. The water is discarded, leaving the wet mash, which is used to cook porridge . This method of preparation is also practiced in certain parts of Ghana, where the cooked porridge is called koko .
3. In Uganda and other southern African countries, dry maize or sorghum is milled into flour with out the soaking step. This is cooked into a porridge, to which an old stock of fermented porridge is added as a starter for fermentation to produce obusera .
The basic process, which involves the enzymatic activities of lactobacilli. Ieuconostocs, pediococci. yeasts. and moulds, is the same, however. The metabolic activities of these organisms result in the production of fatty acids such as lactic, acetic, butyric, formic, and propionic acid. The pH of the foods is reduced to a value of 4.0 or less (see FIG. 1. pH changes during the preparation of fermented Ghanaian maize dough. A = changes due to soaking; B = changes due to fermentation (Source: Ref. 25)). In the fermentation of uji, a final pH of 3.5-4J) at a titratable acidity of 0.6% as lactic acid is produced. The fermentation of cassava for the production of gari results in reductions in pH to 4.0 or less. Neutral compounds such as acetoin, ethanol, and 2,3-butanediol are formed by organisms such as enterobacters, serratiae, and erwiniae. The production of some antimicrobial substances as a result of fermentation has also been reported [24: 25; 30]. All these could contribute to the safety as well as the acceptable flavour of these foods.
TABLE 2. Microbes involved in the fermentation of some
|Maize||ogi||Corynebacterium sp Clostridium sp., Rhodo torula sp.|
|kenkey, koko, akasa||Enterobacter cloacae, Acinetobacter sp., Lactobacillus plantarum, L. brevis, Saccharo myces cerevisiae, Candida mycoderma|
|nasha||Streptococcus spLacro bacillus sp., Candida sp Saccharomyces cerevisiae|
|uji||Leuconostoc mesenter oides, Lactobacillus plantarum|
|Millet||busa, ogi||Lactobacillus plantarum, L. delbrueckii. Sac charomyces busae|
|mahewu||Streptococcus lactis , Lacto -|
|bacillus delbrueckii, L. bulgaricus, L. acido philus|
|Cassava||gari||Lactobacillus plan tarum, Streplococcus sp.|
|Rice||idli||Leuconostoc mesenter oides, Streptococcus faecalis, Pediococcus cerevisiae|
Source: Ref. 28
Fermented foods as a source of nutrients
Improved taste and acceptability
Although taste and food acceptability are not nutritive factors per se, we mention them here for convenience. The desire for more palatable foods than the bland unfermented products could have resulted in the evolution of fermentation as a food-preparation technology. These foods have characteristic flavours and aromas representative of diacetyl acetic acid and butyric acid which make them more appetizing. Some speculative evidence shows that these foods are more acceptable to the anorexic child. Van Veen and Steinkraus  noted that temper, a fermented soybean product, has little of the typical soy-bean flavour and this makes it more acceptable than the raw material.
Viscosity and energy intake
Effective increases in energy density are associated with reductions in viscosity, and fermentation reportedly reduces the viscosity of some foods. Porridge cooked from fermented cassava flour has a lower viscosity than the product from unfermented flour . This reduction is probably due to the activities of amylase-producing micro-organisms that break starch down into simpler sugars, releasing bound water and thus reducing viscosity.
Table 3 provides data on the viscosity of porridge cooked from maize dough at varying stages of fermentation. Porridge cooked from meal prepared from maize grain that had been soaked for 24 hours (pH 4.5) had a lower viscosity than that prepared from dry maize flour (pH 6.2). There was no further reduction in viscosity when the meal was allowed to ferment for 24 hours with reduction in pH to 3.3. The arrest of the reduction in viscosity after further fermentation was perhaps due to the decrease in pH. The activities of amylases are reduced at pH values below 4.0. Gallat  found some decrease in viscosity when sorghum porridges were fermented after cooking but no reduction if a raw flour-and-water slurry was fermented before cooking. Here again the reduced pH could be the limiting factor. An additional hypothesis is that fermentation breaks down carbohydrates into simpler sugars which do not have the matrix configuration for amylase activity.
TABLE 3. Changes in viscosity of porridge cooked from maize dough at different stages of ferment at ion
Wolfe et al.  reported that food such as fermented maize dough could satisfy the energy requirements of the healthy child in Ghana. In a recent study, also carried out in Ghana, it was shown that fermented maize dough porridge could sustain the growth of the partially breast-fed infant if introduced early enough . Most of these studies have been laboratory-based. Large-scale investigations on the effect of fermentation on viscosity and energy intake at the community level are indicated.
Protein and amino acids
The effect of fermentation on levels of protein and amino acids is a topic of much debate. Nanson and Fields  noted improvements in the concentrations of available lysine, methionine, and tryptophan during the fermentation of corn meal. In another study. riboflavin and niacin increased with the fermentation of maize dough . An investigation of the nutritive value of sorghum kisra bread showed no increases in threonine or lysine, but tyrosine and methionine levels did increase . Mbuga  analysed the amino acid content of uji and noted significant increases in riboflavin and tryptophan but a significant drop in lysine. In another study, fermentation significantly improved the percentage relative nutritive value (protein quality) as well as the level of lysine in maize, millet, sorghum, and other cereals . A natural lactic acid fermentation of rice meals produced significant increases in isoleucine and lysine and in the relative nutritive value of riboflavin; niacin and thiamine decreased significantly, however . Padhye and Salunkhe  showed substantial increases in the nutritional quality of proteins in a fermented rice and black gram blend (idli). Fermentation reduced the total crude protein by about 4%-6% in fermented millet products . It appears therefore that the effect of fermentation on the nutritive value of foods is variable, although the evidence for improvements is substantial. The mechanism by which fermentation improves the levels of proteins and amino acids is not clear, but the high concentrations of microbe protein in these foods could be a contributory factor.
Availability of iron and other di- and trivalent cations
Cereals usually have high levels of phytates, which bind cations such as iron and zinc into mineral phytates. These are complexes of low solubility and therefore reduce the availability of these essential minerals. It appears from the limited available literature that fermentation could improve the availability of these minerals. White sorghum-based slurries that were subjected to lactic acid fermentation showed increases in iron availability. The level of iron doubled when dehulled flour was fermented. A sixfold increase occurred when a combination of germination and fermentation was employed. These increases correlated with reductions in phytates, and the authors postulated the activation of enzymes that hydrolysed phytates . Reddy and Salunkhe  also showed that fermentation of rice for only eight hours could result in complete hydrolysis of phytates. Simultaneous increases in the quantity of non-phytates were also noted in the same study. In our own studies, fermented Ghanaian maize dough has shown significant reductions in phytate from 9.9 µm per gram to 4.7 µm per gram after fermentation for 48 hours, a reduction of 20% in phytate concentration.
All these studies were conducted in vitro and measured total phytates. Since the lower phytates do not reduce mineral absorption and there are other substances besides phytates which modify mineral absorption, it is essential to carry out in vivo experiments on the effect of consumption of fermented foods on zinc and iron bioavailability.
Health-related effects of fermentation
The two toxigenic substances of concern in infant feeding are aflatoxins and hydrocyanic acid. Aflatoxins are mycotoxins produced by strains of Aspergillus flavus and related fungi. Optimal conditions for the growth of these fungi and toxin production in contaminated foodstuffs are high humidity and temperature, both of which are common in tropical countries. Enough cereal is stored for consumption throughout the year, which allows for contamination by fungi and hence aflatoxin production. Few studies have evaluated the effect of fermentation and other food-preparation technologies on levels of aflatoxin.
Dada and Muller . investigating the fate of aflatoxin B1 during the production of a fermented sorghum-based porridge from Nigeria, found that the levels of the aflatoxin were reduced considerably. This reduction was coupled with the detection of the less-toxic aflatoxin B2.
Unlike aflatoxin, hydrocyanic acid occurs naturally in certain species of cassava and other foods. In an investigation of the effectiveness of traditional Nigerian fermentation processing methods in reducing HCN to innocuous levels , HCN was reduced from 90.1 mg per kilogram of freshly grated pulp to 55.8 mg per kilogram after fermentation for 48 hours. In another study, fermentation of germinated sorghum for 24 hours reduced the levels of HCN by 70% .
Microbial quality of weaning foods
The antimicrobial properties of fermented foods appear to be their most interesting quality. Evidence on the antimicrobial effect of a variety of fermented foods has increased in recent times. Fermented sorghum-based porridge from Lesotho [47; 48], maize flour from Kenya . maize dough from Ghana [28; 50], and soy-bean tempeh from Indonesia  have demonstrated antimicrobial action against a variety of diarrhoeal pathogens.
TABLE 4. Summary of findings on the inhibitory activity o fermented foods on bacteria
|Fermented food||Organisms inhibited|
|Maize dough||Shigella flexneri  Shigella flexneri, ETEC  gram-negative bacteria |
|Sorghum||Salmonella typhimurium |
|Motoho||Shigella boydii, Salmonella typhi, Escherichia coli |
|Tempeh||Bacillus subrilis, Klebsiella pneumo niae, Staphylococcus aureus [51 ]|
|Fish silage||Staphylococcus sp., coliforms |
|Sausage||Staphylococcus aureus |
|Milk||Staphylococcus aureus, Escherichia coli  Campylobacter jejuni  Vibrio cholerae |
An in vitro investigation in Mali on the antimicrobial effect of a mixture of curdled goat's milk and millet gruel on Vibrio cholerae showed complete inhibition of the organisms after six hours of fermentation, but they survived in gruels without the curdled milk . It would be prudent to limit the use of curdled milk to those communities that have existing traditions for the production of fresh milk, however.
One factor that could produce this antimicrobial activity is the reduction in pH that occurs during fermentation. Most enteropathogens are particular in their pH requirements (table 5); for example, E. coli, shigellae, and salmonellae can survive a minimum pH of about 4.5 and a maximum between 8.0 and 9.0 . Campylobacter jejuni survives acidic pH of around 3.0 [58; 59]; experiments with yoghurt, however. have shown that C. jejuni was inhibited although the pH was between 4.2 and 5.3 .
TABLE 5. Approximate pH tolerance of some microorganisms
|Minimum pH||Maximum pH|
Sources: Refs. 57-59.
That pH per se may not be the only determining factor for the antimicrobial activity of fermented foods has been demonstrated in studies we have carried out in Ghana . Fermented and unfermented maize dough showed no inhibitory activity, but maize dough that had been fermented for three days inhibited shigellae and ETECs by eight hours. Fermented maize dough cooked into porridge showed a reduced antimicrobial effect despite an acidic pH of 3.3. Further studies showed the presence of an antimicrobial substance optimally active at pH 3.1 .
At the community level, fermentation of maize dough reduced the proportion as well as the level of gram-negative bacteria in weaning-food samples collected from mothers in a Ghanaian village . It is of great importance to evaluate the microbial quality of a variety of fermented cereal gruels in order to ascertain their role in producing weaning foods of acceptable microbial quality. In most communities fish, peanuts, and beans are often added to fermented cereal gruels in order to increase nutrient intake. It is therefore also important to investigate the effects of such supplementation on the antimicrobial activities of these fermented foods.
Most investigators have studied the gram-negative enteropathogens, but other bacteria such as Bacillus cereus deserve particular attention. Further studies on the effect of a wide variety of fermented foods on C. jejuni as well as other enteropathogens are also required.
Do fermented foods reduce diarrhoea?
Animal experiments to a large extent have shown that tempeh-formulated food increases the resistance of the gastrointestinal tract to enteropathogens . Nevertheless, the promotion of convenience foods has resulted in the total neglect of the development of most traditional food-preparation technologies. Indeed, some health workers in developing countries have discouraged the use of fermented foods in infant feeding . The use of unfermented foods has been found to be disadvantageous in the feeding of diarrhoeal patients. During the early hours of fermentation. considerable amounts of free sugars are produced, giving the food a sweet taste. If the concentration of these sugars exceeds 2%. there is an osmotic effect, resulting in increased stool output and thus creating problems among children with diarrhoea. Most mothers therefore preferred to feed porridge that has been fermented for at least 24 hours. Mothers interviewed in two Ghanaian villages also used maize dough that was fermented for at least 24 hours , perhaps for the same reason.
It is quite clear that fermentation of weaning foods can inhibit a number of gram-negative enteropathogens, thus improving the foods' microbial quality. By this means, one of the most important routes of transmission of diarrhoeal pathogens to young children could be eliminated. In addition to the potential benefit of fermented foods in increasing the safety of weaning foods, they may also improve the resistance of the gut. Bacteria such as lactobacilli ferment most foods and have metabolic products similar to the indigenous gut flora . These metabolites, if consumed in fermented food, can augment protection against gut colonization by invading pathogens. Indonesians with chronic diarrhoea fed a fermented soybean-formulated diet recovered after 2.39 days as compared to 2.94 days for those given a commercial rice-milk formula . There seem to be no documented investigations on the role of fermented foods in reducing the incidence, duration, and severity of acute diarrhoeal diseases in the community.
Besides providing protection against diarrhoeal pathogens, some, but not all, fermented foods meet the energy and nutrient requirements of the young child. These foods therefore have a significant role in feeding young children, especially in environments with little or no sanitation.
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