FERMENTED MEAT PRODUCTS OF THE WORLD

Fermented foods and beverages are one of the indispensable components of the dietary culture of every community in the world. Traditional fermentation, and smoking, drying, and salting processes were developed by ancient people to preserve foods for consumption, a remarkable step in the food culture history of human beings. Wine was believed to be made in the Caucasus and Mesopotamia as early as 6000 BC, and the colonization by Romans spread winemaking all over the Mediterranean. The antiquity of Chinese foods and cuisines has been documented by several historians as far back as 4000 BC based on historical evidence. The ancient monuments of Nepal indicate that Himalayan ethnic foods have been consumed in the region for more than 2500 years. Food prepared by different communities is unique and distinct due to the geographical location, environmental factors, food preference, and the availability of plant or animal sources. 
Approximately 50–400 g per capita of fermented foods and alcoholic beverages are consumed daily worldwide, representing about 5%–40% of the total daily food intake. Low-cost, high-value, and socially and culturally acceptable fermented foods and beverages are consumed as staple foods, currries, stews, side dishes, fried foods, cooked foods, pastes, seasonings, condiments, pickles, confectioneries, salads, soups, desserts, savories, drinks, candied foods, masticators, colorants, tastemakers, and alcoholic and nonalcoholic beverages. About 5000 varieties of unlisted major and minor fermented foods and beverages are prepared and consumed by billions of people belonging to different communities and ethnicities across the world.

11.1 Introduction

Meat is highly nutritious but, in its fresh state, is perishable and can be an agent for the transmission of a range of infections and intoxications. Not surprisingly, therefore, meat was a subject of the earliest conservation methods developed by humankind. These depended largely for their effect on the reduction of water activity (aw) through removal of available water by drying and salting. This had the effect of controlling growth of normal spoilage microflora associated with the meat but did not necessarily eliminate microbial growth entirely.
In the absence of the normal spoilage bacteria, lactic acid bacteria (LAB) in particular were able to grow, especially where there was a moderate reduction in aw. Their growth enhanced the preservative effect of the reduced aw and improved the sensory properties of the product in terms of texture and flavor. They also contributed to improved safety compared with the fresh raw materials. Products such as raw hams are sometimes described as fermented meats, although in this case the process is largely enzymatic; any bacterial metabolism involved is not fermentative and its effect can usually be reproduced by replacing nitrate with nitrite in the curing salts.

11.2 History

A number of authors have discussed the origin of fermented meats in antiquity (Pederson 1971, Adams 1986, Zeuthen 2007). It appears that an important point of origin was in the Mediterranean region where the process was particularly favored by the warm, dry climate. Fermented meats are usually presented in the form of a sausage, a name that is derived from the Latin salsus, which means salted. Some authors have associated the term salami with Salamis, an ancient city on the Mediterranean island of Cyprus, although it seems more likely that the etymology is related to the Italian sale (salt). Historically, several advances in food processing such as canning and irradiation have been closely associated with military needs, and this seems to have been a factor in the development and dissemination of fermented meats.
The advantages of high nutritional value, good keeping qualities, and portability made dried sausages an important part of the Roman legionaries’ rations as they marched throughout Europe (Shephard 2000). Production of fermented meats seems to have spread from the Mediterranean to Northern Europe from where migration established production in the United States, South America, Australia, and elsewhere (Adams 1986). While this probably represents the main current in the history of fermented meats, it is seldom the case that good ideas occur entirely in a single place and there are products such as the undried, fermented sausage nham and other products from Thailand ; urutan, a Balinese traditional fermented sausage (Antara et al. 2002); and salami-type sausages produced in several regions of China that clearly suggest the independent development of related products elsewhere.

11.3 Classification

Fermented sausages comprise chopped or ground meat that is mixed with other nonmeat ingredients such as curing salts, spices, and flavoring components, and allowed to undergo a lactic fermentation in the course of a drying process. In its essentials, the production of fermented sausage is similar to that of cheese making; both involve salting, drying, and lactic acid fermentation and the products are generally eaten without cooking. Based on these relatively simple processing steps and widespread artisanal production, numerous fermented meats have been developed, in many ways comparable to the plethora of different cheeses available throughout the world. As with cheeses, the most useful system of classification for such a diversity of products is based on their moisture content giving rise to three groups of products: dried, semidry, and undried. Further subdivision is possible based on additional aspects of processing such as whether the product is smoked and/or mold ripened (Lücke 1998).

Himalayan dish including ethnic yak sausage

An account of the fermented foods of Thailand (Phithakpol et al. 1995) describes a number of different fermented meat products. These usually employ beef or pork, and, as with many European-style products, the slight differences in formulation or processing gives rise to a number of different products. One notable feature of some of these products is their relatively low fat content compared with European fermented meat products. The Himalayan people have a variety of traditionally processed smoked, sun dried, air dried, or fermented meat products including ethnic sausages from yak, beef, pork, sheep, and goats (Tamang 2010). Yaks (Bos grunniens) are reared in alpine and subalpine regions between 2100 and 4500 m altitude in the Himalayas for milk products processed ethnic meat products of the Himalayas are kargyong, satchu, suka ko masu, kheuri, chilu, chartayshya, jamma, and arjia (Rai et al. 2009). These are naturally cured without starter cultures or the addition of nitrites/nitrates.

11.4 Preparation

The ingredient mix plays a crucial role in determining the distinctive qualities of a particular product and numerous variations in formulations exist. Typically for a European-style fermented meat, it would comprise
Lean meat                                 55%–70%
Fat (lard)                                   25%–40%
Curing salts                                 3%
Fermentable carbohydrate          0.4%–2%
Spices and flavoring                    0.5%
Others (starter culture, acidulant, ascorbic acid) 0.5%

In principle, the meat from any animal could be used to produce a fermented product. There are reports of exotica from sources such as horse, deer, ostrich, and yak (Tamang 2005, Capita et al. 2006, Vural and Özvural, 2007) but pork, beef, mutton, and poultry are the most common. The meat and fat are minced or chopped prior to mixing with the other ingredients in a bowl chopper. These operations are best performed at low temperatures (about -4°C) to avoid smearing of the meat particles with fat. In most European-style fermented meats, failure to do so would give an aesthetically undesirable appearance since discrete meat and fat particles would not be discernable. Covering meat particles with fat may also impede the drying process and give rise to microbiological problems subsequently. Curing salts are generally a mixture of two or three different salts and play a major role in directing the fermentation process, and ensuring good texture, flavor, and color in the product.
The most abundant of the salts is sodium chloride. At least 2% is required to give the product its necessary gel texture by solubilizing the myofibrillar proteins in the meat during initial mixing. Sodium chloride also restricts the growth of the normal meat spoilage flora, which is largely comprised of relatively salt-sensitive gram-negative organisms such as pseudomonades, while allowing growth and acid production by the more halotolerant LAB. In addition, it is an important component of the product flavor. The beneficial role of nitrate or nitrite in curing appears to have been a fortuitous discovery as a result of using salt (sodium chloride) contaminated with potassium nitrate. It was later found that nitrate acts simply as a reservoir from which nitrite can be produced by bacterial reduction so sodium nitrite or a mixture of sodium nitrite and potassium nitrate are often used now.
The nitrite produces the characteristic red color of cured meats following reduction to nitric oxide, which complexes with the red meat pigment myoglobin to produce nitrosomyoglobin. It contributes to flavor by acting as an antioxidant and has a significant effect on the safety of the product by inhibiting the growth of a range of pathogenic organisms, most particularly Clostridium botulinum, Listeria monocytogenes, and Salmonella. Nitrite itself is toxic and so the levels used are strictly regulated. In the EU, the amounts of nitrite and nitrate that can be used in meat curing are currently restricted to 150 mg/kg potassium nitrite and/or 150 mg/kg sodium nitrate (European Commission 2006). However, the level of nitrite found in products declines markedly during ripening and storage due to a number of reactions competing with those already described such as addition reactions with amino acids and unsaturated fatty acids, and oxidation.
The risk that nitric oxide could react with secondary amines leading to the production of carcinogenic N-nitrosamines has attracted considerable attention.
Under current conditions of practice, this does not appear to be a matter for concern. The increasingly common ingredient, ascorbate, inhibits nitrosamine formation which in any event appears low, as indicated by a number of product surveys (Adams 1986, Silla-Santos 2001, Honikel 2007). A wide array of different herbs and spices are included at the mixing stage, the precise make up of this mixture depending on the product type. Common ingredients would be mustard, black pepper, garlic, nutmeg, pimento, mace, and coriander. They are added primarily as flavoring ingredients and as such play an important role in conferring the particular character of individual products; for example, the smoked paprika added to the Spanish or Portuguese chorizo or the bird peppers added to nham in Thailand. However, it is now recognized that they do make other contributions to the keeping quality of the product.
They often contain a range of phenolics, many of which will have antioxidant properties. These and other metabolites present in spices and herbs also have antimicrobial effects that can contribute to the inhibition of the normal spoilage flora while allowing the generally less-sensitive LAB to grow. The antimicrobial activity of herbs and spices has been a subject of considerable research effort in recent years, but, in the most part, this has been restricted to descriptive studies on the effect of individual products and their effect on particular organisms, generally pathogens (see, for example, Nychas and Skandamis 2003). More detailed knowledge will be required before this activity can be used in a predictable and directed way.
If herbs or spices are used as the native plant material rather than derived oleoresin preparations then this can further benefit the fermentation. Extracts of clove, cardamom, ginger, celery seeds, cinnamon, and turmeric, all with relatively high manganese content, have been shown to stimulate lactic acid fermentation, an effect which increases with increased manganese content (Zaika and Kissinger 1984). It is thought that manganese helps protect LAB, lacking the enzyme superoxide dismutase, from the damaging effects of reactive oxygen species such as superoxide (Archibald and Fridovich 1981). Once the ingredients are mixed, the sausage batter, as it is sometimes called, is packed into its casing. Traditionally, natural collagen from the intestinal tract of animals is used, but this has been increasingly replaced by regenerated collagen casings produced from the corium layer of cattle hides.
In addition to possessing the desirable properties of being permeable to moisture to allow drying, being able to adhere to the sausage mix so that the casing shrinks with the drying sausage, being permeable to smoke, and being digestible, regenerated collagen casings have the advantage of relative abundance of supply and uniformity of properties compared to intestinal casings. Casings made from cellulose produced from wood pulp may sometimes be used as these possess very similar properties, although they are indigestible and have to be removed before the product is consumed. Nham is packed in plastic film and/or banana leaves. European fermented sausages tend to be fermented at lower temperatures and for longer periods than those produced in the United States. This can be as low as around 10°C for some Hungarian and German sausages (Lücke 1998) but is usually below about 26°C.
The higher fermentation temperatures in the United States (27°C–38°C) give a faster fermentation, although there is an increased risk of pathogen growth occurring should it be present. The relative humidity during fermentation is generally 85%–90%, 10% lower than the equilibrium relative humidity (ERH) of the sausages. Care is taken to match the rate of moisture loss from the surface of the sausage to migration of water from within the sausage so that case hardening does not occur. After the fermentation or ripening stage, which typically lasts 1–3 days, the sausage is dried at 7°C–15°C for up to 6 weeks at a relative humidity dropping from 85% to as low as 65%, depending on the target moisture content of the product. In a fermented meat such as nham, which does not undergo drying, the fermentation takes place at around 30°C for 3–5 days.

11.5 Microbiology—Functional Microorganisms and Safety

In meat fermentations, the selective effect of the environment and processing conditions is vitally important in ensuring a satisfactory fermentation. Many products still rely on this entirely to ensure the growth of the required organisms from within the natural microflora of the ingredient mix. This can be assisted by a procedure known as back-slopping where mix from a previous successful batch is retained and added to the new batch to ensure the introduction of a substantial, healthy inoculum. Even where commercial starter cultures are used, the selectivity of the environment plays a significant role since, unlike in many fermented dairy products, it is not possible to pasteurize the raw materials to eliminate competitors. In terms of the microflora associated with successful fermentations, LAB are probably preeminent since they are invariably involved in the production of all the fermented meats described here, and increase to levels of around 108 cfu/g during the course of fermentation.
Other groups of organisms are important in some products as described below but generally achieve levels in the range 104–106 cfu/g. Numerous studies have been conducted identifying the particular species of LAB associated with different fermented meats. Lactobacillus (Lb) species are dominant at the end of fermentation with the most common species encountered being Lb. sake, Lb. curvatus, and Lb. plantarum (Leroy et al. 2006). With nitrate cures, which are nowadays more common in Europe than in the United States, gram-positive, catalase-positive cocci such as Staphylococcus xylosus, Staph. carnosus, Staph. saprophyticus, and Kocuria varians (formerly known as Micrococcus varians) are important for the reduction of nitrate to nitrite. They will also produce a number of significant aliphatic flavor compounds through the degradation of amino acids and fatty acids (Stahnke 1999, Stahnke et al. 2002).
These organisms would normally be most active at the start of fermentation and tend to be inhibited as the LAB begin to dominate and the pH declines. Of the fungi, yeasts are commonly encountered in fermented sausages but their numbers are usually relatively low. They do, however, appear to contribute to the product flavor and decrease its acidity. Molds are particularly suited to aerobic conditions, and reduced pH and water activity at the surface of a fermented sausage, and mold ripening by Penicillium, Aspergillus, Mucor, Eurotium, and Cladosporium species is a feature of some products. This is especially true for those from Southern Europe that are ripened for long periods and not smoked, where a white covering of mold is a characteristic feature. Studies of naturally mold-ripened sausages have sometimes reported isolation of potentially mycotoxigenic fungi (Leistner 1984, Larson et al. 2001).
In one recent study of Italian sausages, about 45% of 160 samples examined were positive for the presence of the mycotoxin ochratoxin A. The toxin was associated with the surface casing; none was detected in the meat itself and the toxin could be removed by brushing or washing the sausages (Iacumin et al. 2009). Concern over the possibility of mycotoxin production has prompted the more widespread use of nontoxigenic mold starter cultures in those products where mold ripening is required. These mostly employ Penicillium species (the genus most frequently associated with naturally ripened products) such as P. nalgiovense (Leistner 1990). Where surface mold growth is not required it can be prevented by smoking, dipping in sorbate or natamycin (pimaricin), or by vacuum packaging. Bacterial starter cultures have been used in fermented meats for about 50 years (Adams 1986, Jessen 1995).
Freeze-dried Pediococcus acidilactici, a strong acid-producing strain, was introduced in the United States as being particularly suited to the quicker, higher temperature fermentations employed there, whereas the first starter culture introduced in Europe was a Micrococcus (now Kocuria) primarily for nitrate reduction. Since then, more subtle combinations of starters have been introduced and deep-frozen products are available that simplify handling and give a more rapid initiation of fermentation. The benefits of starter use have been demonstrated on numerous occasions and for many product types including the Turkish soudjouk and Thai nham (Kaban and Kaya 2006, Visessanguan et al. 2006). In addition to Pediococcus species, which are generally not commonly found in naturally fermented meats, Lactobacillus species such as Lb. plantarum, Lb. sake, and Lb. curvatus are also available.
These are often derived from characteristic isolates of natural fermentations. They are classed as facultatively heterofermentative lactobacilli that breakdown hexoses, such as glucose, homofermentatively to produce mainly lactic acid but are also capable of heterofermentation of pentoses via phosphoketolase when glucose levels are depleted to produce a mixture of lactic and ethanoic acids. Gram-positive, catalase-positive cocci such as Staph. carnosus, Staph. xylosus, and Kocuria varians are also available to reduce nitrate to nitrite, giving rise to the desired color and other effects, but their catalase activity also helps stabilize the color against oxidative destruction by peroxide. Fermented meats are an archetype of what has been described as the hurdle or multiple barrier concept of food preservation in which the overall antimicrobial effect seen is the aggregate result of a number of antimicrobial factors.
In the case of fermented meats, the keeping quality and safety depend on the reduced water activity/salt, nitrite, the antimicrobial effect of herbs, and the activity of the LAB. These hurdles do not all apply at the start of processing but accumulate sequentially as processing proceeds (Leistner and Gould 2002). Of these, the LAB have attracted considerable attention since their acceptability as food additives would make any antimicrobial effect they achieve acceptable too. The antimicrobial activity of LAB has been periodically reviewed often with much attention focused on the relatively minor antimicrobial factors (Adams 2001). However, the central feature common to all LAB is their ability to produce organic acids and decrease the pH as an inevitable consequence of their growth. This is their most important contribution to meat fermentation where, at some stage of the process, they decrease the pH, typically, to a value around 5.2 (although this varies considerably between different products).
One antimicrobial factor other than organic acid that, if not generally significant in meat fermentations, may be important in particular cases and may be worth incorporating more widely in starter cultures is the ability to produce bacteriocins. Bacteriocins are proteins or polypeptides produced by bacteria that are inhibitory, usually to closely related species. The precedent for using a bacteriocin in fermented foods comes from the accepted and widespread use of nisin, a bacteriocin produced by strains of Lactococcus lactis, in products such as canned foods and processed cheese. Nisin is unusual in that it has a wider range of activity than most bacteriocins since all gram-positive bacteria are sensitive and bacterial endospores are particularly so.
Nisin and other bacteriocins with similar properties could be expected to have a protective effect against gram-positive pathogens in fermented meats such as L. monocytogenes, Staph. aureus, and Clost. botulinum, though they would of course inhibit other gram positives such LAB and micrococci that might play some positive role in the fermentation. There have been reports of the relative benefits of adding nisin to fermented sausages (Hampikyan and Ugur 2007) and numerous reports of the production of bacteriocins by LAB isolates from fermented meats (see, for example, Tichaczek et al. 1992, Garriga et al. 1993, Rattanachaikunsopon and Phumkhachorn 2006, Belgacem et al. 2008, Xiraphi et al. 2008). This has also led to the employment of bacteriocin-producing starters in sausage fermentations and the demonstration of useful inhibition of Listeria species (Leroy et al. 2006, Ammor and Mayo 2007).
Though some fermented meats are given a final pasteurization treatment to eliminate any pathogens that may be present, many rely entirely on the antimicrobial hurdles described above to assure safety. The epidemiological data on outbreaks caused by fermented meats suggest that three bacterial pathogens are the major concerns: Salmonella (Taplin 1982, Van Netten et al. 1986, Cowden et al. 1989), Staph. aureus (Barber and Deibel 1972, Metaxopoulos et al. 1981, Warburton et al. 1987), and verotoxin- producing Escherichia coli (VTEC) (Anon 1995a,b, Conedera et al. 2007, Sartz et al. 2008). A similar conclusion was drawn from a hazard identification exercise conducted for fermented meats by Beumer (2001). This is further supported by surveillance data from two independent surveys conducted in the United Kingdom in the late 1990s, which showed remarkably similar findings.
VTEC was not detected in a total of almost 3500 independent samples, although Salmonella was found at similar levels in both surveys; 2 out of 2981 samples in one and 1 out of 455 samples in the other. The levels of Staph. aureus were greater than 102/g in 1.3% and 1.1% of samples in the two surveys (Adams and Mitchell 2002). Although considerable research effort has been devoted to L. monocytogenes in fermented meats, there appear to have been no outbreaks reported. Only one of the two surveys described above looked for L. monocytogenes, and it was detected in 3% of 455 samples but only at levels below 102/g (Adams and Mitchell 2002). As a result of the outbreaks of VTEC associated with fermented meats, the U.S. Food Safety Inspection Service required producers to validate that their production process could achieve a 5-log reduction in viable numbers of E. coli O157.
This was based on a worst case scenario, and several products were unable to achieve this goal with their existing process (Beumer 2001). A review of the results of these trials concluded that if E. coli O157:H7 is present in sufficient numbers, it is able to survive a range of fermentation and drying processes. Typically the reduction achievable in most processes was 2–3 log cycles and it could be less in some cases. The European fermentation method with its longer fermentation at a lower temperature gave better reductions as did high salt, high nitrite, and low pH (Getty et al. 2000).

11.6 Nutritional Aspects

The composition and nutritional value of fermented meats has been discussed recently (Demeyer 2007). Though they offer a range of valuable nutrients and vitamins, fermented meats also enjoy the negative aspects of high fat and salt contents, which are associated with cardiovascular diseases, hypertension, and a number of other conditions common in relatively affluent societies. In some cases, there are options for reducing the level of these components. Reformulation to achieve lower fat by adopting products such as nham as a model is one obvious approach for European and North American fermented meat producers. Improving the quality of the fat used by using fat from animals fed a diet to increase unsaturated fat levels has been tried, although the product was more susceptible to oxidation and the development of rancidity. Other trials using vegetable oils rather than animal fat as an ingredient seem to have enjoyed slightly more success (for a review, see Ansorena and Astiasarán 2007).
The critical role that salt plays in the texture, flavor, and microbiological stability of fermented meats appears somewhat more difficult to replace. Decreasing salt will result in losses of these qualities, and the use of alternatives such as potassium chloride and potassium lactate has enjoyed limited success (Ansorena, Astiasarán 2007). On a more positive note, the potential of fermented sausages as a vehicle for probiotic bacteria has been investigated, although their potential health benefits remain to be fully clarified. It may be that established starter organisms used in meat fermentations already possess probiotic potential. Alternatively, it might be possible to incorporate established probiotic strains in fermented meats (Leroy et al. 2006, Ammor and Mayo 2007, Ansorena and Astiasarán 2007). They might then play some useful part in the fermentation process or the product could simply act as a carrier for the probiotic strain and help protect it from stomach acidity in its passage through the gut.

11.7 Conclusion

Fermented meats originated independently in a number of regions around the world, although European-style products now predominate in terms of their scale of production and the degree to which they have been subject to scientific scrutiny. The original objective of meat fermentation was to preserve an otherwise very perishable product, but with the advent of alternative preservation methods the distinctive sensory properties of the products have assumed greater importance, particularly in the developed world. Studies conducted on fermented meats from other regions frequently reveal their similarity to other, better-known products in terms of their microbial composition and the changes that take place during fermentation/drying. However, in certain key areas such as nutritional and sensory properties, there may be unique aspects which we can learn from and possibly apply more widely in the future.

From the book 'Fermented Foods and Beverages of the World, edited by Jyoti Prakash Tamang and Kasipathy Kailasapathy, CRC Press- Taylor & Francis Group, U.S.A, 2010, p. 309-319. Adapted and illustrated to be posted by Leopoldo Costa.

Share this post