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Review Article
Fermented Meat Products: Organoleptic Qualities and Biogenic Amines-a Review

V.P. Singh, V. Pathak and Akhilesh K. Verma
Fermented foods are value added products which have higher nutrients, prolong shelf life and easy in digestibility and are more suitable for the intestinal tract. The organoleptic qualities of such foods are higher particularly in terms of flavour, taste, aroma and colour. For the production of fermented products we require starter culture such as Lactic Acid Bacteria (LAB) strains, most of the meat starter cultures are Lactobacillus pentosus, L. casei L. curvetus, L. planterum, L. sakei, Pediococcus acidilactici and P. pentosaceus. These foods are also able to produce certain biogenic amines; the most commonly found biogenic amines in the meat and meat products are tyramine, cadaverine, putrescine and also histamine. The formation of such bioamines further enhances the functional properties of the foods besides addition in nutrients.
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V.P. Singh, V. Pathak and Akhilesh K. Verma, 2012. Fermented Meat Products: Organoleptic Qualities and Biogenic Amines-a Review. American Journal of Food Technology, 7: 278-288.

DOI: 10.3923/ajft.2012.278.288

Received: November 20, 2011; Accepted: January 18, 2012; Published: March 20, 2012


Fermented foods are those which are subjected to the act of microbes or its enzymes for induction of useful biochemical changes and significant modification in foods (Campbell-Platt, 1987). However, Microbiologist describes the fermentation as a form of energy-yielding microbial metabolism in which an organic substrate, generally a carbohydrate, is partly oxidised and an organic carbohydrate acts as the electron acceptor (Adams, 1990). This explanation means that processes regarding ethanol production by yeasts or organic acids via Lactic Acid Bacteria (LAB) are believed as fermentations. Fermented foods are those foods which are infected or overgrown by safe to eat micro-organisms whose enzymes, mainly amylases, proteases, lipases hydrolyse the polysaccharides, proteins and lipids to harmless commodities with flavours, aromas and textures pleasurable and appealing to the human consumer (Singh and Sachan, 2011b). If the commodities of enzyme actions have objectionable odours or undesirable, unappealing flavours or the products are poisonous or disease producing the foods are considered as spoiled.

In the South East Asia the fermented food product is known as the sour meat give the impression to be increasing in fame as consumer search for further varieties in their food choices. Meat products that inoculated with micro-organisms at the time of processing under controlled condition to develop desirable characteristics are known as the fermented meat products (Acton, 1977). However, generally local producers depend on natural fermentation without inoculation or any controlled condition (Singh and Sachan, 2009; Singh and Sachan, 2011a). In such case, the micro-organisms present in these products normally originate from the meat itself or from the environment. Fermentation of meat imparts five major functions in meat products such as:

Improvement in human nutritional through development of a spacious diversity of flavours, aromas and textures in foods
Preservation of considerable amounts of food by the use of lactic acid, alcoholic, acetic acid, alkaline fermentations and high salt
Enhancement of food qualities in terms of vitamins, proteins, essential amino acids and essential fatty acids
Detoxification through food fermentation processing
Reduction in cooking times and energy requirements

Origin of fermented meat products: Fermented sausages perhaps originated in the Mediterranean region during Roman period. Some products like Salami Milanese and Hungarian Salami have succeeded for centuries and are till now day being consumed. The process of fermentation was carried out throughout centuries without any scientific information regarding the nature of the processes involved in the fermentation of meat products. Recently, sausage-manufacturer would transfer old curing brine to the newly-prepared one. As a result novel brine would become inoculated with useful micro-organisms, causing the important changes in the cured meat at the time of ripening. This conventional process was depended on practical observations without the information of bacteriology (Singh and Sachan, 2010a). So, the results were not forever acceptable.

In 19th century, Pasteur reported that fermentations are completed by particular types of organisms. The first definite bacterial starter cultures, proposed for the fermentation of milk, were introduced during 100 years before.

Benefits of fermented meat products: Fermentation of meat is a low energy process which brings various changes in the meat products such as natural acidulation, preservation modus operandi which gives exclusive and characteristic meat properties such as flavour and palatability, colour, microbiological safety, softness etc. Antioxidant properties of phenolic compounds exert various antibacterial properties, flavour, colour etc. (Amadou et al., 2009; Chukeatirote et al., 2010; Qazi et al., 2003). In the process of fermentation, raw meat changes into the fermented meat products by the ‘cultured’ micro-organisms with the help of lower the pH of the meat products. The reduction in pH lowers the water activity (aW) and creates the microbial hurdles which help in producing a safe and sound product. Fermented meat products commonly have a long storage life due to added salt, low pH due to lactic acid formation by LAB in the early stages of storage and afterwards drying that reduces the water activity (aW). The beneficial effects of fermented meat products may be summarized as:

Increase the demand of consumption of the meat products due to the improvement in the flavour, taste, aroma and colour
Fermented meat products have long storage life as compared to non fermented meat products due development of acidulation at the time of fermentation
Fermented meat products are safer from dangerous and pathogenic micro-organism because starter culture inhibit their growth in fermented meat products
Fermented meat are more tender (soft) as compare to non fermented due to activity of certain enzyme (like protease etc.) produced by the starter culture
The nutritional status of these foods is high due to production of peptides, amino acid at the time of fermentation
For the fermented meat products less cooking time is required as compared to non fermented meat food which saves the energy and cost of production

Starter culture for meat fermentation: Hammes and Knauf (1994) defines the meat starter cultures as the “preparations that include living or inactive micro-organism that build up the desired metabolic activity in the meat”. As an act, they are of facultative hetero fermentative strains of micro-organisms which form lactic acid from hexose sugars, for e.g., glucose and lactose as their metabolic products (via glycolysis). Though, from pentose, such as arabinose and xylose they formed both lactic acid as well as acetic acid (through the 6-phasphogluconate/phasphoketolase pathway) (Kandler, 1983). The formation of the amount of acetic acid is typically 1/10th of the amount of lactic acid (Deketelaere et al., 1974). As designated in industrial catalogues of Lactic Acid Bacteria (LBA) strains, most of the meat starter cultures are Lactobacillus pentosus, L. casei L. curvetus, L. planterum, L. sakei, Pediococcus acidilactici, P. pentosaceus. Starter culture Micro-organisms for Fermented Meat products are presented in Table 1.

Fermented meat products: Meat and meat products are consumed in almost all communities of the World. Meat is one of the richest food sources of protein (Lucke, 2000). However, it gets easily contaminated by pathogenic micro-organisms present in animals prior to being slaughtered. It is therefore important to make meat safe for consumers in terms of stability, transportation and storage (Singh and Sachan, 2010b). One of the preferred methods used to achieve these qualities is meat fermentation. Fermentation of meat sausages, for example, using selected LAB strains, strongly inhibited the spoilage bacterial growth but left the organoleptic properties of the products intact (Metaxopoulos et al., 2002; Aderiye et al., 2006). Thus, LAB strains can be effectively used to preserve meat products for quality purposes. Lanhouin, a fermented fish product consumed by the locals in the West African country of Benin (Anihouvi et al., 2006) is processed by spontaneous and largely, uncontrolled fermentation. The product was found to be safer and free of pathogenic bacteria such as Salmonella. It has also been demonstrated that fish products, which were LAB fermented could be stored for longer periods, free of the fishy odour and taste (Gelman et al., 2000).

Table 1: Starter culture Micro-organisms for fermented meat products (Hammes and Knauf, 1994)

Table 2: Role of micro-organisms in fermented meat products

Furthermore, the nutritional quality of fish remained intact (Achi et al., 2007). Role of micro-organisms in fermented meat products is enlisted in Table 2.

Formation of different aroma compounds in fermentation
Aroma compounds from carbohydrate degradation:
At the time of fermentation most of the supplementary carbohydrate is transformed into lactic acid. The formation of different amounts of other products depending on the applied lactic acid bacteria, temperature, type and content of carbohydrate and other processing parameters (Bhattacharya and Das, 2010; Adebayo and Aderiye, 2010). Other than lactic acid bacteria some starter cultures like staphylococci or yeast also have some effects in changing sugars to products other than lactic acid. At the time of fermentation of sausage some volatile compounds were formed from carbohydrate catabolism such as acetic, propionic and butyric acids, acetaldehyde, diacetyl, acetoin, 2, 3-butandiol, ethanol, acetone, 2-propanol and more (Gottschalk, 1986; Demeyer, 1982; Stahnke, 1999; Awan et al., 2003). However, pyruvate derived compounds may originate from many sources other than carbohydrate during microbial metabolism (Demeyer et al., 1987).

Aroma compounds from protein break-down: During the process of fermentation of sausages extensive proteolysis takes place which forms peptides and free amino acids. At the time of maturation amino acids and small peptides are taken up by the micro-organisms and transformed into numerous aroma compounds by different pathways. Some important biochemical conversions of the amino acids such as leucine, isoleucine, valine, methionine and phenylalanine take place into the sensory important branched aldehydes and corresponding secondary products, such as acids, alcohols and esters (Montel et al., 1998; Stahnke, 2000; Shah et al., 2002). The changes are mainly due to micro-organisms species from the Micrococcaceae family. Some worker also reported that both in model experiments and in sausages that different staphylococci and Micrococci (kocuria) produce 2, 3-methylbutanal, 2-methylpropanal, 2, 3-methylbutanoic acid, 2-methylpropanoic acid, 2, 3-methylbutanol, ethyl 2, 3-methylbutanoate, methional, phenylacetaldehyde, phenylethanol and many more (Berdague et al., 1993; Stahnke, 1994; Stahnke, 1999; Montel et al., 1996; Masson et al., 1999; Larrouture et al., 2000). The quantity of compounds is extremely influenced by the processing circumstances. In sausages it has been shown that parameters such as temperature, pH, glucose, salt, nitrite, nitrate and ascorbate all influence the amount of aroma compounds in one way or the other (Stahnke, 1995b, Stahnke, 1999; Masson et al., 1999; Larrouture et al., 2000). It has also been reported that due to reaction between the corresponding amino acids and adiketone such as diacetyl (nonenzymatic Strecker reactions) the branched-chained aldehydes were formed in this reaction (Stahnke, 1995b; Barbieri et al., 1992). Some other workers describe the presence of different pyrazines in unspiced fermented sausages (Stahnke, 1995b; Johansson et al., 1994; Berdague et al., 1993).

Aroma compounds from lipid catabolism: At the time of fermentation and maturation the lipid fraction of the sausage is moderately hydrolysed by lipolytic reactions in which triglycerides and phospholipids are liberating free fatty acids. Lipolysis has been widely studied since free fatty acids are assumed to be chief precursors for oxidation products of significance for flavour development. Recent study designate that due to the microbial-oxidation of free fatty acid methyl ketones are formed which may be important for maturity (Stahnke, 2000) but possibly the quantity of free fatty acids is so plenteous that augmented amounts of this precursor do not control the flavour profile. Aroma compounds are present in the ppb to ppm levels whereas the level of free fatty acids are between 0.5 to 7% depending on sausage type (Nagy et al., 1989; Stahnke, 1994; Johansson et al., 1994; Navarro et al., 1997).

There are two method of lipolysis that is caused both by microbial enzymes and endogenous enzymes in the meat and fat and there has been much debate about which mechanisms are the dominant. However, the current study illustrate that the addition of antibiotics is a most important component of the lipolytic breakdown and is documented to endogenous enzymes in the presence of strong lipolytic strains of Staphylococcus are used as a starter culture (Molly et al., 1997; Stahnke, 1994). It has also been reported in sausages that the amount of free fatty acids is increased by high fermentation temperature and reduced salt levels (Stahnke, 1995a).

Occurrence of biogenic amines in meat and meat products: Meat and meat commodities have commonly been reported to contain biogenic amines (Bover-Cid et al., 2006; Galgano et al., 2009; Hernandez-Jover et al., 1997; Kanioua et al., 2001; Ruiz-Capillas and Jimenez-Colmenero, 2004). Among these different biogenic amines, the most commonly biogenic amines found in the meat and meat products are tyramine, cadaverine, putrescine and also histamine (Ruiz-Capillas and Jimenez-Colmenero, 2004). Therefore, an opposite relation between spermidine and sperminet contents is a characteristic of foods of animal source as compared with plant commodities (Kalac and Krausova, 2005). Occurrence of few amines such as tyramine, putrescine and cadaverine is a normal phenomenon at the time of storage of meat products (Galgano et al., 2009; Hernandez-Jover et al., 1996). The concentration of tyramine in stored beef was found more at the surface so on washing the concentration reduced (Kanioua et al., 2001; Paulsen et al., 2006). Fermented meat commodities comprises of significant amounts of biogenic amines but the draw back is poor quality raw materials, contamination and unsuitable conditions during processing and storage. In addition, the micro-organisms responsible for the fermentation process also imparts the biogenic amines accumulation (Bover-Cid et al., 2006; Latorre-Moratalla et al., 2010; Ali, 2010; Gernah et al., 2011). The accumulation of the non-protein nitrogen in the fermented meat products includes the free amino acids, precursors of biogenic amines. Naturally raw meat acts as the substrate from which the biogenic amines are formed. It is also a biggest part of the matrix in which the decarboxylation reactions take place and any circumstances that change its nature and characteristics will influence the formation of biogenic amines (Ruiz-Capillas and Jimenez-Colmenero, 2004). Many authors such as Eerola et al. (1997), Komprda et al. (2004) and Maijala et al. (1995) reported the formation of the biogenic amines considerably different in fermented meat commoditise and it is depends mainly on the raw material hygienic quality. Though, the level of the amine is depending on the raw material, presence of decarboxylating micro-organisms either from ecological contamination or from inoculation culture and the environment supporting their growth and activity. The quantity of amines and its profiles depends on various factors through manufacturing process such as pH, Nacl, redox potencial and temperature, the size of the sausage, sanitary conditions and importance of starter cultures (Gardini et al., 2001; Komprda et al., 2004; Latorre-Moratalla et al., 2008; Omafuvbe, 2008). Among these factors pH is a chief factor that influences amino acid decarboxylase activity. The formation of the amine is certainly influenced by the temperature. The optimum growth for the most of decarboxylase containing bacteria is in between 20 and 37°C temperature and the reduced temperature inhibit their growth (Karovicova and Kohajdova, 2005). Comparatively less concentration is committed to the effect of the chemical substances supplementary during made of the fermented meat products. Even though the recognized antimicrobial properties of some spices, the direct assessment of an effect of spices on microflora in association with biogenic amines making it present in accessible literature (Komprda et al., 2004). Suzzi and Gardini (2003) reported that the concentration of biogenic amines decreases obviously with increase of Nacl concentration, at the same time proteolytic activity is much higher for middle concentration of salt, pointing out that there is not essentially an association between these two variables. According to the Karovicova and Kohajdova (2005), the existences of Nacl stimulate tyrosine decarboxylase activity and hamper histidine decarboxylase activity. A correlation can also be established between biogenic amines substance and the size of dry fermented sausages. The size (diameter) of the sausage affects the surroundings in which micro-organisms grow; for e.g., the salt content is normally low and water activity is high in sausages having large diameter. The high production of the certain amines, such as putrescine and tyramine is possibly due to larger diameter. Usually, the level of the biogenic amines is higher in the thicker diameter of the sausage as compared to the thinner diameter sausage and in the mid portion of the sausage than the rim of the sausage (Ruiz-Capillas and Jimenez-Colmenero, 2004; Suzzi and Gardini, 2003).

Role of starter culture in formation of biogenic amines: The selection of appropriate starter culture with amino oxidase activity is the basic in preventing the development of high levels of biogenic amines in fermented meat products (Karovicova and Kohajdova, 2005; Suzzi and Gardini, 2003). The choice of lactic acid bacteria for the meat fermentation is dependant on the particular needs of the fermentation process (J. Stadnik, Dolatowski), (Roig-Sagues and Eerola, 1997). The incapability of the culture to form biogenic amines, capability to grow well at the temperature proposed for processing of the manufactured goods and competitiveness in diminishing the development of wild amine producing microflora should be taken into concern in the selection of starter cultures (Suzzi and Gardini, 2003). The formation of curvacin A by the bacteriocin strains may enhance the competitiveness (Hammes and Hertel, 1996; Somda et al., 2011). A fast pH diminishing caused by amine negative starter cultures is able to basically stop biogenic amines growth in fermented meat products. Furthermore, starter cultures capable to compete among non-starter bacteria during the ripening and storage can further avoid too much biogenic amines production (Suzzi and Gardini, 2003). For the increase of the acidification in the fermented meat products is primarily due to the lactic acid bacteria along with the micrococci and/or coagulase-negative staphylococci. They are responsible for addition of colour and aroma due to their proteolytic and lipolytic actions. Thus the micro-organisms commonly used in the meat industry as inoculation culture (Latorre-Moratalla et al., 2010; Suzzi and Gardini, 2003). In Europe commonly used strains are the Lactobacillus curvatus and Lactobacillus sake as compared to the other. Though, a number of strains of Lactobacillus curvatus can be used as starter cultures to form four different biogenic amines. Strains of Lactobacillus sake are free from this potential (Koiozyn-Krajewska and Dolatowski, 2009). It indicates that Lactobacillus sake is more appropriate than Lactobacillus curvatus for use as a starter culture to stop the development of biogenic amines (Roig-Sagues and Eerola, 1997).

Present and future of fermented meat products: In genetic engineering use of recent starter cultures for bioamines products and product development is a new area. In the future by the use of genetic engineering we can get better production and activity of microbial protease, lipase, catalase, nitrate reductase. By this technique we can give newest properties, or make stronger the popular ones already present in the microbe. By the use of this technology it is also possible to transfer the new gene from one to other micro-organisms. So that it can generate aroma components, vitamin, certain desirable metabolites and so on. In addition to investigation oriented in the direction of the result of old, conventional trouble of meat fermentation, there are new elegant methods to produce superior cultures with stronger activity that favour a good fermentation process can be evolved. A lot of study has been conducted in the field of meat fermentations. However, we are away from the thoughtful entire interrelations involving the microbiology, the technology and external factors use in fermentation and ripening procedure.


On the basis of above discussion it can be concluded that the fermentation of foods in particular meat and meat products enhances its nutritional value. The products prepared by fermentation can keep for a longer period of time. The biogenic amines produced through fermented foods may serves the functions of functional foods. The sensory attributes alongwith the digestibility are quite higher in fermented foods as compared to traditional foods.

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