2. Literature review

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2.1 Introduction
2.2 Microbiology of fermented fishery products
2.3 Chemical changes during fish fermentation
2.4 Quality and marketability of products
2.5 Safety

2.1 Introduction

Fermented fish have, for many years, been considered as a Southeast Asian product. These products are highly salted and fermented until the fish flesh is transformed into simpler components. Fish fermentation in the Southeast Asian sub-region normally lasts for several months (three to nine months) and the fish flesh may liquefy or turn into a paste (Huss and Valdimarson, 1990). Some of these products include nuoc-mam of Vietnam and Cambodia, nam-pla of Thailand, sushi of Japan and patis of the Philippines. No African fermented fishery products are mentioned in the FAO Fisheries Report No. 100 on fermented fish; however, fessiekh from the Sudan is mentioned as a Mediterranean product.

In Africa salting and drying of fish for preservation is accompanied by fermentation, but the period is short (a few days) and the product is not transformed into a paste or sauce. The products are all characterized by a strong odour and, for this reason, various authors have described the product as "sink" fish. In Ghana fermented fish is called momone, an Akan word which literally means stinking. The "stink" fish of Sierra Leone has been described (Watts, 1965) as fish which had developed a strong odour within 24 hours of capture and was salted for about four days and then dried. Watanabe (1982) described the fermented fishery products of Senegal as highly salted and semi-dried fishery products with an obnoxious odour and a cheesy but rich fishy flavour reminiscent of kusaya from Japan. The characteristic smell of fermented fish is the result of enzymatic and microbiological activity in the fish muscle. Zakhia and Cuq (1991) suggest that the organic acids produced during the fermentation of fish in Mali are mainly acetic acids, whereas it would appear that in Asia mainly lactic acid is produced.

Fermented fish is, therefore, any fishery product which has undergone degradative changes through enzymatic or microbiological activity either in the presence or absence of salt.

2.2 Microbiology of fermented fishery products

Fish in its natural environment has its own micro-flora in the slime on its body, in its gut and in its gills. These micro-organisms, as well as the enzymes in the tissues of the fish, bring about putrefactive changes in fish when it dies. Furthermore, the micro-organisms generally present in the salt used for salting also contribute to the degradative changes in the fish.

Figure 1 Growth Ranges of Micro-organisms with respect to Water Activity

Micro-organisms require water in an available form for growth and metabolism. Figure 1 shows that all microbial growth is inhibited at water activity (A_w) below 0.60. Halophiles grow optimally at high salt concentrations but are unable to grow in salt-free media. Halotolerant organisms grow best without significant amounts of salt but can also grow in concentrations higher than that of sea water. Xerophiles are those organisms which grow rapidly under relatively dry conditions or below A_w of 0.85 while osmophiles can grow under high osmotic pressure. Most food-borne bacterial pathogens are not able to grow in an A_w range of 0.98-0.93 Table 1).

Various types of salts are used for the salting and fermentation of fish. They include solar salt, rock salt and vacuum salt and have their own micro-flora. Solar salt, which is the most widely used in fish curing, has been found to contain the largest amount of micro-organisms. The general bacterial flora of solar salt mostly comprises bacillus types (75 percent) with the remainder being micrococcus and sarcina types. The most important spoilage organisms always present in solar salt are the red halophilic bacteria.

In the degradative changes occurring during fermentation no significant changes were observed in the amino-acids particularly the essential ones. The degradation process, however, brings out certain characteristic flavours which are essential for the quality of the final product (Amano, 1962; Ito and Sato, 1963).

Table 1 - Growth of Micro-organisms in Salted Fish

Staphylococcus aureus grows poorly in competition with the natural micro-flora of most foods at high levels of water activity.

Source: Microbial Ecology of Foods, 1980, Vol.1, Chapter 4

Most fermented fishery products are made from fatty fish. Lean fish has sometimes been noted to give a less acceptable texture and flavour. The role of fats in the fermentation process has not, however, been studied in any detail. Fish oils are highly unsaturated and hence very prone to oxidation. Certain pro-oxidants, such as haem, in the proteins catalyze the oxidation reaction. Similarly, iron impurities in the crude solar salt used for curing also accelerate auto-oxidation (Saisithi, 1967). Oxidized fish oils have a characteristic taste and paint-like smell, but the acceptability of products having the typical taste and flavour of oxidized fats depends very much on local preferences. The products of fat oxidation take part in further reactions especially with amines (Saisithi, 1967) and with other decomposition products of proteins (Bal and Dominova, 1967) to produce coloured compounds as well as substances with odour Jones, 1966). Lipases present in the fish flesh also hydrolyze the lipids (Lovern, 1962), but the extent is dependent on the level of salting and fermentation (Amano, 1962).

Pathogens rarely multiply at high salt concentrations, however, Karnop (1988) demonstrated that Pediococcus halophilus is able to produce histamine during long storage at ambient temperatures of 20°25°C. Toxins produced by Clostridium botulinum in poor quality fish before salting may be stable in the salted product (Huss and Rye-Petterson, 1980).

Krieg and Holt (1984) noted that the red halophiles belong to two genera of bacteria, namely Halobacterium and Holococcus. Halobacterium consists of rod-shaped bacteria and requires at least 1015 percent salt concentration for growth whilst Halococcus can thrive at 5-10 percent salt concentration. Both genera are strictly aerobic and grow optimally at about 37°C and also produce red carotenoid pigments.

In situations where brine is reused a number of times, the chemical composition of the salt solution is altered. Significant amounts of organic material are introduced and the bacterial load of the brine becomes extremely high, especially the red halophiles and the osmophilic moulds. Two common defects of salted fermented fishery products called pink and dun are the result of spoilage by red halophilic bacteria and a highly osmophilic fungus respectively. The red halophilic bacteria grows in brine solutions at temperatures ranging from 15° to 55°C. Table 1 shows that only a few pathogenic organisms can proliferate at salt concentrations higher than 10 percent. However, it is known that many of these organisms survive in saturated salt solutions. For instance, Typhus bacteria can survive in saturated salt solutions for three to six months, salmonella in 10 percent salt solutions for one to three months. Escherichia cold and Staphylococcus aureus can survive for many weeks in salted fish (ICMSF, 1980).

A study by Knochel and Huss in 1984 on the microbiology of barrel salted herrings revealed that both aerobic and anaerobic viable counts (in media containing 15 percent sodium chloride) were low, i.e. not more than 3 x 105/g of fish. The types of micro-organisms identified were:

(i) gram-negative aerobic halophilic rods (70 percent);
(ii) gram-positive aerobic halotolerant cocci (20 percent);
(iii) yeasts (3 percent).

Villar et al. (1985) also showed that Pediococcus halophilus is the dominating organism in salted anchovies.

2.3 Chemical changes during fish fermentation

Several studies have been carried out to study the biochemical pathways followed during the degradation process of fish fermentation. Reay and Shewan (1949) reported that the strong odour in spoilt fish may be a reaction between TMAD and lactic acid producing TMA and acetic acid. Tomiyasu and Zenitani (1957) also incriminated organic acids in deteriorated fish. Pearson (1962) identified the following five chemical changes in deteriorating fish:

(i) enzymic degradation of nucleotides and nucleosides in the flesh leading to the formation of inosine, hypoxanthine, ribose, etc.;

(ii) bacterial reduction of trimethylamine oxide (TMAO), a non-volatile and non-odoriferous compound, to volatile trimethylamine (TMA) which has an amoniacal smell;

(iii) formation of dimethylamine (DMA);

(iv) breakdown of protein with subsequent formation of ammonia (NH₃) indole, hydrogen sulphide, etc.;

(v) oxidative rancidity of the fat.

Hiltz et al. (1976) reported that the volatile bases particularly TMA, DMA and NH, are associated with changes in the organoleptic and textural quality of fish.

The development of a specific aroma in fermented fish sauces and pastes may not be due to the action of micro-organisms. In a recent study, Adams (1986) concluded that micro-organisms play little or no part in aroma production. Beddows (1985) isolated halotolerant organisms, Bacillus sp. (cocci) and used them in pure culture but none of them produced the typical Fish sauce aroma.

It can therefore be concluded that the microbiology of any salted, dried or fermented fishery product is greatly influenced by the natural micro-flora of the fish, the salt and the conditions under which processing takes place.

2.4 Quality and marketability of products

Formal quality control systems are entirely lacking in the artisanal fish processing industry. Poor quality fish (i.e. stale, heavily infested, broken or mouldy) has a low market value (Beatty, 1969; Mills, 1979). Very high quality products on the other hand do not necessarily attract a correspondingly high value in local markets. Various studies on quality in relation to prices (Disney, 1974; Breslin and Hoffman, 1975) did not show any evidence that the best cured fishery products fetch higher market prices. Watanabe and Mensah (1976) could not correlate retail prices and organoleptic quality for salted dried fish in Ghana. Hara and Mkoko (1990) considered the local (Malawi) market for traditional cured fishery products a seller's market: a market characterized by scarcity, limited price competition and cartels). Notwithstanding this observation, a good quality cured fish is relatively easy to sell at the optimum market price as compared to a similarly priced inferior product.

It is always desirable to use good quality raw materials in the production of cured fishery products. However, the general practice, particularly with fermented fishery products, is that processors resort to fermentation as a last attempt to salvage deteriorating fish especially during periods of glut when other traditional processing methods such as smoking cannot cope with the volume of the catch.

Consequently, unwholesome or inferior quality raw fish is often processed into fermented products which are, however, acceptable by traditional quality standards.

2.5 Safety

2.5.1 Hygiene of processing

Boats, premises, fishermen, processors, equipment, water, fish and ingredients are invariably of low hygienic standards at the artisanal level of fish handling and processing. This may be attributed to a lack of facilities, services, education, standards (and their enforcement) and - most important a lack of economic support from the quality products' market.

2.5.2 Histamine poisoning

Histamine poisoning results from the ingestion of foods containing high levels of histamine (Taylor, 1983 and 1986). This poisoning has historically been referred to as scombroid poisoning because of the frequent association of the illness with the consumption of spoiled scombroid fish such as mackerels and tuna. Also sardines, herrings, pilchards, anchovies and shellfish have been implicated in histamine poisoning. Histamine poisoning has also been reported in connection with non-fish fermented foods like cheese and sauerkraut (Taylor, 1986). In Africa, data on the incidence of histamine poisoning is scanty because incidents are often not reported. Japan, the UK and the USA are countries where food poisoning from fish consumption is often reported. Less frequent incidents have also been reported in Australia, Canada, Egypt, France, Indonesia, the Netherlands, New Zealand, Norway and Sri Lanka (Taylor, 1986; and Abdalla, 1989). Public health officials in many other countries, including African countries, have admitted that histamine poisoning occurs but is not officially reported.

Histamine production in foods is by the decarboxylation of histidine through a reaction catalyzed by the enzyme histidine decarboxylase. Geiger, Courtney and Schanakenberg (1944) reported that histamine was generated from autolysis. Recent research, however, indicates that the decarboxylation reaction results largely from bacterial action (Arnold and Brown, 1978; Ababouch et al., 1991a). These reports indicate that the fermentation of fish is a likely source of histamine. Various species of fish are known to have large amounts of free histidine in their muscle tissues as substrate for histidine decarboxylase. Ababouch et a!. (1991b) noted that proteolysis, whether autolytic or bacterial, may play a role in free histidine release.

Histidine decarboxylase has been found mainly in certain species of Entero-bacteriaceae, Clostridium and Lactobacillus (Taylor et al., 1978; Frank, 1985). Enteric bacteria have been found to be the most important histamine forming bacteria in fish. Morganella morganii, Klebsiella pneumoniae, Proteus vulgaris and Hafnia alvei are, however, the only histamine forming bacteria that have actually been isolated from fish implicated incidents of histamine poisoning (Frank, 1985).

The threshold toxic dose (TTD) for histamine is not precisely known and it is difficult to establish because of its varying levels in spoiled fish. In studies conducted by Simidu and Hibiki in 1955, it was estimated that the TTD for histamine in fish is approximately 60 mg/100g. Due to the . in determining the TTD, several countries have adopted maximum allowable levels of histamine in fish. The US Food and Drug Administration (FDA), for instance, established a hazard action level (HAL) of 50 mg/100g in tuna products based on the investigation of previous histamine poisoning outbreaks and the defect action level (DAL) of 20 mg/100g.

The EEC 1993 Health Regulations for Fishery Products are expected to introduce a DAL of 10 mg/100g and a maximum allowable limit of 20 mg/100g (EEC, 1990), but there are no defined guidelines for histamine levels in Japan and the UK although there are many reported cases of histamine poisoning in these countries.

2.5.3 Clostridium poisoning

Since the fermentation process involves bacterial activity, it is likely that if conditions are not properly set to control pathogenic bacteria they may remain in the fermented products. This is because fermentation takes place at low temperatures. The two main factors which control the growth of pathogens such as Clostridium botulinum are high salt concentration and pH. All types of C botulinum are inhibited by 10-12 percent salt and a pH below 4.5. C botulinum types E, F and non-proteolytic type B are able to grow between 8° and 10°C but are inhibited below 4°C. From observations of the production methods of fermented fishery products, the low level of incidence of C. botulinum poisoning may be mainly attributed to the high level of salt usage. Furthermore, toxins of micro-organisms such as C botulinum are inactivated by proteolytic enzymes. Since there is some proteolytic activity in the fish fermentation process, it is therefore most likely that C bondinum toxins may be inactivated.

Incidents of poisoning from fish consumption may be low in Africa because, despite the high initial microbial load of fermented fishery products, foods are generally cooked with intense and prolonged heat.

In a study on fessiekh processing, Abdalla (1989) reported that the pH of the product ranges from 6.4 to 6.9 and the salt level is 6-7 percent (fresh weight). These are favourable conditions for the growth of C botulinum and other proteolytic bacteria. This could possibly be the reason for fatalities involving the consumption of fessiekh in Egypt where the raw product is a delicacy among some people.

2.5.4 Salmonella poisoning

There is very little information on salmonella food poisoning arising from the consumption of fermented fish in Africa despite the unsanitary fish processing practices observed in many countries.

In a study conducted by Nerquaye-Tetteh et al. (1978) to isolate various micro-organisms, no Salmonella spp. were isolated from samples of fermented fishery products obtained from the open markets in Ghana. The absence of Salmonella spp. from fermented fishery products could be attributed to the high salt level and low water activity of the products. These conditions do not favour the growth of salmonella.

Furthermore, traditional food preparations in Africa involve a long period of cooking. Since Salmonella spp. are heat labile, they are destroyed during intense cooking.

2.5.5 Mould infestation

Moulds are able to grow under dry conditions better than bacteria. For this reason, moulds are often associated with dried fermented fishery products. Spores of moulds which are often present in the air and soil contaminate fish during processing. Insects and mites are also known to cause mould contamination by carrying the spores on their bodies.

The moulds commonly associated with dried cured fish in storage are Aspergillus halophillus; A. restrictus; Wallemia sebi; A. glaucus group; A. candidus; A. ochraceus; A. flavus and Penicillum spp. (Christensen and Kaufmann, 1974).

Dun, which is a defect associated with cured fish, results from mould growth on fish with an A_w of 0.75 and salt concentration of 10-15 percent. It does not produce any objectionable flavour or change in texture in the fishery products. The main problems are, however, its visible growth and the discoloration product. Some strains of mould produce harmful mycotoxins in dry food products. The toxin of greatest health concern is aflatoxin produced by Aspergillus flavus and A. parasiticus. Various researchers have reported dangerous levels of aflatoxin in dried fish (Okonkwo et al., 1977). Townsend et al (1971) isolated A. flavus from Vietnamese cured fish and identified it as responsible for producing aflatoxin. Christensen and Kaufmann (1974) noted that all mould growth is influenced by temperature. The optimum temperature for mould growth is 30°C and the maximum ranges from 40° to 55°C depending on the species. These are typical ambient temperatures in tropical regions.

Reported incidents of aflatoxin poisoning in Africa are rare, probably due to the long period of heating during food preparations or lack of records.

2.5.6 Insect and mite infestation

In the early stages of curing, raw fish is particularly susceptible to infestation from blowfly maggots (larvae). Fully or partially cured fishery products are also attacked by a wide range of insect pests which include species of flies, mites and both adults and larvae of certain beetles.

Insect and mite infestation of cured fish is greatly influenced by factors such as the temperature, moisture content, ambient relative humidity and salt level of the product. Improper disposal of fish waste and offals, and unhygienic surroundings provide favourable breeding grounds for these pests.

2.5.7 Use of chemicals in fish curing

Common salt (sodium chloride) is the most widely used chemical in fish curing in many African countries. However, in the technologically advanced countries, other substances such as benzoic, boric, sorbic and acetic acids as well as sodium benzoate may be added to the salt solution to enhance preservation. Sugar and starch have also been reported as substances which are added to fish during curing to enhance fermentation.

2.5.8 Pesticides used for preservation

In recent times, fishermen and processors in Africa have resorted to the use of organic insecticides to catch or preserve fish. Azeza (1986) reports that in the Lake Chad basin substances such as Lindane, Shelltox, Gardona and DDT are used to prevent insect infestation of cured fish. Unfortunately, these chemicals are used without any strict control over the safe dosage levels, hence the product though protected from insects could be harmful to consumers.

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