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Food Research International 27 (1994) 299-307

Fermented meat products

Friedrich-Karl Liicke
Microbiology Laboratory, FB Haushalt & Erniihrung, Fachhochschule Fulda, PO Box 1269, D-36012 Fulda, Germany

This paper provides general information on the fermentation of meat, the types
and manufacture of the resulting products, the microorganisms involved and
the factors affecting microbial activity. Subsequently, recent developments in
the following three main research fields are reviewed: (i) Instrumental control of
meat fermentation: Sensors for continuous measurement of fermentation para-
meters such as pH, water activity and weight loss of fermenting meats have been
developed, making the on-line control of the fermentation climate feasible. This
could lead to a marked reduction in fermentation time and costs without affect-
ing product quality. (ii) Selection of antagonistic lactic starter cultures: Such cul-
tures, ideally, would kill rather than inhibit pathogens, not only in fermented
meats sensu strict0 but possibly also in non-fermented products such as sliced
perishable meats. (iii) Role of microorganisms in flavour development: A better
understanding of the effect of microorganisms (in particular Micrococcaceae
and their ability to scavenge oxygen, destroy peroxides and hydrolyze lipids and
proteins), meat enzymes and non-enzymic reactions on aroma and flavour of
fermented meat is required to maintain a large diversity of fermented meats and
to improve their sensory quality and shelf life.

Keywords: fermented meat, microbial activity, instrumental control, starter


cultures.

INTRODUCTION: WHAT ARE FERMENTED Historically, it appears that the first fermented
MEAT PRODUCTS? sausages were made in certain parts of the
Mediterranean. This may be due to the fact that a
According to the definition given by Campbell- proper climate (temperature and relative humid-
Platt (1987), a food is termed ‘fermented’ if it ‘has ity) is crucial for the drying process, and fairly
been subjected to the action of microorganisms or stable wet and cool conditions prevail there dur-
enzymes so that desirable biochemical changes ing the winter. Nowadays, more than 700000 t are
cause significant modification of the food’. This ap- produced and consumed within the EEC and
plies to most types of raw sausages and raw hams. EFTA countries each year, particularly in Ger-
Fermented sausages are defined as ground meat many, Italy, Spain and France (Liicke et al.,
mixed with salt and curing agents, stuffed into 1990). Production figures in the New World are
casings and subjected to a fermentation process in much lower: in the United States, about 153 000 t
which microorganisms play a crucial role. Most dry and semi-dry sausages were produced in
fermented sausages are dried and can be stored USDA-certified plants in 1981 (Adams, 1986).
with little or no refrigeration. In Europe, the There are few traditional fermented meat products
manufacturing pracess does not include a final in Asian and tropical countries, ‘nham’ (a meat
heat treatment although some varieties (especially product popular in south-east Asia) being an ex-
fresh raw sausages) are consumed after cooking. In ception (Campbell-Platt, 1987). The Chinese
the United States, fermentation of sausages made sausage of the ‘Lup Cheong’ type is a dried, but
from ‘uncertified pork’ is followed by heating to not fermented meat product (Leistner, 1986a).
58~3°C to kill any trichinella possibly present. Dry cured, unground raw meats are mainly pre-
served by salting and drying, and excellent raw
Food Research International 0963-9969/94/$07.00 hams can be prepared without significant micro-
0 1994 Canadian Institute of Food Science and Technology bial activity. Rather, the activity of meat enzymes
299
300 Friedrich-Karl Liicke

is important for the development of the aroma and From a regulatory point of view, fermented
tenderness of these products. Bacteria are needed sausages are usually subdivided according to their
mainly for the reduction of nitrate which is still fre- raw material (meat type, fat content) and their de-
quently used as a curing agent, and bacteria have gree of drying. These factors make up most of the
also been reported to improve the flavour. In addi- production costs. Criteria are, for example, the
tion, injection of lactic acid bacteria along with sugar water/protein ratio or, as in Germany, the content
has been suggested in order to lower the pH of hams of collagen-free protein.
and facilitate water removal. Accordingly, some bat Table 1 indicates the parameters that the proces-
terial strains are available or have been suggested as sor may vary in order to produce different prod-
starter cultures (see Hammes, 1986; Leistner & ucts. There is a large variety of fermented sausages,
Lticke, 1989; Lticke et aZ., 1990, for reviews). and consumer preference varies considerably be-
Some perishable meat products may also be tween countries, even between different regions
preserved by addition of selected strains of lactic within Germany. For example, ‘sour’, smoked,
acid bacteria antagonistic to pathogens and semi-dry sausages are well accepted in countries
spoilage flora (see Lticke & Earnshaw, 1991, for a like the US or The Netherlands while consumers in
review). Ideally, however, the added bacteria many other countries, particularly in France and
should not change the flavour and appearance of the Mediterranean, do not readily accept smoked
the product. In particular, a large drop in pH is sausages, particularly those with an unbalanced
not desired in meat or most meat products. Such sour taste. In addition, such sausages are more
foods are, by definition, not fermented, and the prone to fat deterioration and less suitable for long-
cultures used are more aptly called ‘protective cul- term storage. Spreadable varieties comprise about
tures’ rather than ‘starter cultures’. 30% of the raw sausages produced in Germany but
Reviews on fermented meats have been provided are uncommon in all other countries.
by Liepe (1983), Bacus (1984), Liicke (1985), Adams
(1986), Leistner (1986a) and Leistner & Liicke
(1989). The present paper will focus on the microbi- SAUSAGE FERMENTATION
ology and technology of fermented sausages.
Meat as a substrate for microorganisms

MANUFACTURE AND TYPES OF In contrast to milk, lean meat contains consider-


FERMENTED SAUSAGES able amounts of peptides and amino acids but
only small amounts of glucose and glucose-6-
For the manufacture of typical dry fermented phosphate (up to 0.15% of each; Dainty, 1986).
sausages, lean meat (60-70%) and fatty tissue The content of these fermentable sugars, as well as
(3040%) are comminuted, mixed with about the content of lactic acid and the pH, depend on
2.43% salt, curing agents, some sugar, spices and, the glycogen content of the muscle at slaughter
in many cases, starter cultures. The mix is placed, and may vary considerably. As a rule, meat with a
with inclusion of as little oxygen as possible, into pH above 59 contains too little lactate and sugar
vapour-permeable casings and subjected to a fer- for a safe fermentation; it binds water tightly and
mentation and drying process. Control of tempera- provides better conditions for growth of acid-
ture and relative humidity is essential for the labile bacteria. Such muscles should be sorted out
production of dry sausages. Ripening chambers and used for other purposes. The same is true for
with precisely adjustable temperature and humidity various muscles of poultry and limits the use of
are expensive, particularly if they are equipped with poultry as raw material for fermented sausages:
smoke generators and smoke combustion devices. according to Holley et al. (1988a), not more than
This is the main reason why today only a small 15% of mechanically deboned poultry meat should
proportion of fermented dry sausages are manu- be added. Furthermore, poultry meat is frequently
factured on an artisanal scale, even in the Federal contaminated with salmonellae. Accordingly, Ger-
Republic of Germany and France with their many man regulations require a minimal ripening time of
small charcuteries. The chambers also require a 4 weeks for raw sausages containing poultry meat.
high energy input, even though this can be reduced Obviously, meat fermentation is a solid-substrate
considerably by using ambient air to control the fermentation with bacteria growing in micro-
relative humidity (Stiebing et al., 1982). colonies (Katsaras & Leistner, 1988). In contrast
Fermented meat products 301

Table 1. Parameters influencing tbe qoality of femmted sausages

Parameter Variables (examples) Guidelines”

Raw material Animal species pH I 5.8; good microbial quality; no antibiotics


(beef/pork/poultry)
Age at slaughter
Fats/oils in pig feed;
Type of fatty tissue (back/belly) No soft or rancid fat
Formulation (fat content)

Additives Sodium chloride Initial a, 0~9554965


Curing agent (nitrite/nitrate) Addition of 100 mg NaNO,/kgb
Sugar amount 0.247%
Sugar type (glucose/sucrose/lactose/dextrins) 0.24.5% of rapidly fermentable sugar
Lactic acid bacteria pH reduction to I 5.3 during fermentationC
Acidulants
Micrococcaceae
Ascorbate
Spices

Comminution Method (grinder/cutter) Low temperature (to avoid melting of fat)


Degree (coarse/fine)

Filling Filling equipment No air inclusions


Casing material (natural/collagen-based/ Permeability high for vapour and smoke, low
cellulose-based) for oxygen; shrinkable, peelable
Casing diameter

Ripening Fermentation climate


- temperature 2 25°C
- time Until pH I 5.3
- humidity (% ERH) No vapour condensation; ERH in
chamber 5-10 units below ERH of product

Ageing/drying climate
- temperature I 15°C until a, < 0.90
- humidity (% ERH) ERH in chamber 10-15 units below ERH of product
- air movement Uniform drying
- time

Surface treatment Smoke No growth of undesired moulds


Mould starter

‘Certain deviations are possible if proper precautions are made (e.g. low ripening temperatures).
bLower amou nt s re q uir’f~lower fermentation temperatures or faster acid formation; use of nitrate instead of nitrite requires lower
fermentation temperature.
Necessary rate depends on fermentation temperature.

to many other fermentation substrates, it cannot smoked products, there is little if any growth of
be pasteurized without changing its appearance other groups of microorganisms: they are inhib-
completely. Hence, any starter culture must be able ited by pH in combination with anaerobic condi-
to compete with the microflora of the raw mate- tions in the interior and by smoke constituents on
rial. The interior of the meat - be it cornminuted the surface, respectively. When acid production is
or not - rapidly becomes anaerobic, which re- slow or delayed, when nitrate rather than nitrite is
stricts growth of obligate aerobes to the surface. used and/or when the products are not smoked,
non-pathogenic catalase-positive cocci may attain
Development of the lmicroflora levels in excess of 107/g at the surface. This is
characteristic for sausage varieties common in the
The conditions prevailing in sausage fermentation Mediterranean and France. The increased risk of
(listed in Table 1) ,strongly favour the lactic acid growth of undesired acid-sensitive bacteria is com-
bacteria. Particularly in rapidly fermenting, pensated for by low fermentation temperatures.
302 Friedrich-Karl Liicke

Table 2. Microorganisms as starter cultures for sausage fermentation (Uicke et al., 1990)

Microbial group Species used as starters” Useful metabolic activity Benefits to sausage fermentation

Lactic acid bacteria L. plantarum, L. pentosus, Formation of lactic acid Inhibition of pathogenic and
L. sake, L. curvatus, spoilage bacteria
P. pentosaceus, P. acidilactici Acceleration of colour formation
and drying

Catalase-positive cocci S. carnosus, S. xylosus, M. varians Nitrate reduction and Colour formation and stabilization
oxygen consumption
Peroxide destruction Delay of rancidity
Lipolysis? Aroma formation
Nitrate reduction Removal of excess nitrate

Yeasts Debaryomyces hansenii Oxygen consumption Delay of rancidity


Lipolysis Aroma formation

Moulds Penicillium nalgiovense Oxygen consumption Colour stability


biotypes 2, 3, 6 Peroxide destruction Delay of rancidity
Lactate oxidation Aroma formation
Proteolysis Aroma formation
Lipolysis? Aroma formation

“Abbreviations: L., Luctobacillus; P., Pediococcus; S., Staphylococcus; hf., Micrococcus.

Species composition and the role of desired selection of formulations (particularly amount and
microorganisms type of fermentable carbohydrate added) and
ripening conditions, manufacturers restrict the ac-
Table 2 lists microbial species available as starters tivity of the lactic acid bacteria to a level which is
for sausage fermentation. Many of these, in par- sufficient to eliminate microbial hazards but does
ticular the psychrotrophic, salt-tolerant LuctobaciZZus not interfere too much with the desired activities of
species L. sake and L. curvatus (see Hammes, the acid-sensitive flora. For the same reasons, cata-
1986, for review), the non-pathogenic Staphylococ- lase-positive cocci are even more frequently used as
cus species S. xylosus (Fischer & Schleifer, 1980; starters than lactic acid bacteria, and many manu-
Delarras & Laban, 198 1; Seager et al., 1986; Sel- facturers prefer Lactobacillus plantayum and pedio-
gas et al., 1988), the yeast Debaryomyces hensenii cocci. At 20-25”C, these form acid more slowly
(Leistner & Bern, 1970; Comi & Cantoni, 1980) than Lactobacillus sake and L. curvatus (Hechel-
and the mould Penicillium nalgiovense (Leistner, mann et al., 1988; Landvogt & Fischer, 1990).
19863) also dominate in the ‘spontaneous’ fermen- The stoichiometry and kinetics of fermentation
tation flora. The role of microorganisms in of Belgian-type (smoked) sausage have been thor-
sausage fermentation is also shown in Table 2. oughly studied by D. Demeyer and co-workers
Sausages may be fermented by lactic acid bacte- (reviewed by Demeyer et al., 1986). They found
ria with little or no participation of catalase-posi- that degradation of amino acids contributes to
tive cocci. This may still result in a product of about lOoh of the metabolized organic com-
acceptable colour and sufficient shelf-life for large- pounds, and that only 60% of these (expressed as
scale production and distribution provided that ni- pyruvate equivalent) are transformed to lactate;
trite is used as the curing agent, peroxide formation 5% end up as acetic acid, and 35% are further oxi-
is avoided and the pH is rapidly lowered to 5-O or dized to CO,. These figures are subject to major
below. Such fermented sausages are common in the variations, the trend being that the absence of
United States, but are also produced in Sweden, oxygen and the addition of defined cultures of lac-
The Netherlands and Belgium. However, con- tobacilli shifts the stoichiometry towards a more
sumers in many European countries, particularly in ‘homolactic’ fermentation. Kinetic studies indicate
France and the Mediterranean, do not readily ac- that this could be due to a much shorter lag until
cept sausages with a plain sour taste. In addition, initiation of acid formation and, consequently,
such sausages are more prone to fat deterioration earlier inhibition of respiratory and/or acetate-
and less suitable for long-term storage. By careful forming bacteria.
Fermented meat products 303

Factors affecting microbial processes sugar. Addition of sugar in excess of about 0.7%
may lead to undesired secondary fermentation dur-
As already mentioned, the onset, rate and extent ing ageing and storage because only at a, values
of acid formation are critical in the manufacture below 0.92 does the rate of acid formation become
of fermented sausages. They must be adjusted negligibly small. Finely ground products of large
carefully to achieve both favourable sensory prop- diameter attain lower pH values than coarsely
erties and safety from pathogens. ground products of small diameter (large
The length of the apparent lag phase before mea- surface/volume ratio; Rodel, 1986) because they dry
surable acid formation depends on the initial num- slower, and the better access of oxygen causes some
ber of lactic acid bacteria adapted to the prevailing shift from lactic acid to CO, and volatile fatty acid
conditions. Addition of lactic acid bacteria (usually formation (van Hoye & Demeyer, 1987).
about 106/g) may shorten the lag considerably, pro-
vided they are sufhciently competitive in the (ini- Use of starter cultures
tially cold) sausage mix and they are not damaged
during harvesting, freezing or lyophilization. In meat fermentations, the effect of adding starter
The initial water activity also affects the onset cultures is smaller than in dairy fermentations be-
and rate of acid formation (Landvogt & Fischer, cause in most cases, sufficient numbers of the mi-
1990). At a, values below 0.955, acid formation croorganisms necessary are present in the raw
may be too slow to inhibit Staphylococcus aureus material. The first defined starter cultures for meat
(Marcy et al., 1985; Hechelmann et al., 1988). How- fermentation were introduced in the early 1960s
ever, at a, values above 0.965, salt-labile pathogens and the use of starter cultures increased in parallel
compete much better, and additional precautions with the need for standardization of the ripening
are needed to suppress these organisms. At initial a, process, the product quality, and the trend towards
values above 0.97, the risk of faulty fermentation shorter ripening times. In the United States, a major
becomes too great (Wirth, 1988). trigger for the widespread use of starters were out-
The rate of acid formation is further determined breaks of staphylococcal food poisoning due to im-
by the type of added carbohydrate, the dominating properly fermented sausages. Lticke et al. (1990)
species of lactic acid bacteria, and the temperature. provided data on the current use of starter cultures
Generally, glucose, sucrose and maltose are fer- for meat fermentation in Europe. In the former
mented rapidly, and lactose slowly, but the different Federal Republic of Germany, for example, virtu-
sugar fermentation pattern of various lactic acid ally all dry smoked sausages with total ripening
bacteria must be taken into account (Hammes et al., times of the order of 3 weeks are produced with the
1990). At 2&25”C, Luctobacillw sake and L. curva- addition of starters, predominantly a combination
tus grow fastest (Hechelmann et al., 1988; Landvogt of a lactic acid bacterium with a Staphylococcus or
& Fischer, 1990) while at 40°C (a temperature Micrococcus strain. There is also a trend towards
sometimes used in summer sausage manufacture in adding such cultures to undried, spreadable raw
the United States), Pediococcus acidilactici is most sausages. Use of defined starters in Mediterranean
active. However, at high fermentation temperatures, countries is increasing, but is less common; this refl-
mesophilic pathogens compete better, and tempera- ects the fact that traditional slow processes benefit
tures above 25°C sbould be avoided unless a very only slightly from the addition of cultures.
rapid pH decline is guaranteed.
Because of their high manganese content, natu-
ral spices tend to increase the rate of lactic acid CURRENT RESEARCH TOPICS AND
formation (Nes & Skjelkvale, 1982; Zaika & FUTURE DEVELOPMENTS
Kissinger, 1984).
The extent of acid formation depends on the Improved control of sausage fermentation and ageing
amount of sugar added, on the rate of drying and
on the development of an acid-consuming surface In commercial practice, both a standard formula-
microflora (particularly on unsmoked products). If tion and a time schedule for the ripening of a
the initial pH is correct (5.8 or below), a pH decline sausage variety is (more or less empirically) devel-
to below 5.3, as normally required for microbiolog- oped. The ripening schedule specifies how long the
ical safety and for optimal drying, can be achieved product remains in which climate. The climate is
by adding as little as 0.2 % of a rapidly fermentable then adjusted by hand or by timers and/or the
304 Friedrich-Karl Lticke

sausages are transferred from one ripening room Much research has been carried out on the fate
to another. In view of the unavoidable variations of S. aureus during sausage fermentation. It
in the raw material and its microbial load, this turned out that at initial ripening temperatures
does not always exclude batch-to-batch variation above 20°C a lactic acid fermentation lowering
in the product. An on-line control of the fermen- the pH to about 5.3 is important for the control
tation and ageing climate could lead to a marked of this bacterium (see Genigeorgis, 1989, for a re-
reduction in ripening time and costs without view). Consequently, the American Meat Institute
affecting the quality of the products. For example, in 1982 specified the maximum time allowed in
once the pH has been lowered to 5.3, fermentation ‘good manufacturing practice for fermented dry or
can be slowed down by lowering the temperature, semi-dry sausage’ to reach pH 5.3 (e.g., 80 h at
and water removal can be speeded up by lowering 24°C). If nitrate was used instead of nitrite, the
the relative humidity. addition of nitrate reducing starters (e.g. Micro-
Sausage fermentation and ageing can be fol- coccus variuns, Meisel et al., 1989) contributed to
lowed by measuring the pH, the water activity, the the suppression of S. aureus. In unsmoked
weight loss and the firmness. Methods for on-line sausages, the risk of growth of S. aureus may be
measurement of the former three parameters have greater because the moulds colonizing the surface
been developed (Rode1 & Stiebing, 1987). An ele- raise the pH, and antimicrobial smoke con-
gant method of controlling the ripening climate is stituents are absent. However, if the fermentation
by measuring the water activity of the sausage sur- temperature is low enough or the rate of acid pro-
face by means of psychrometry (Stiebing & Riidel, duction fast enough, S. aureusis reliably suppressed
1989). The surface a, value, in conjunction with (Metaxopoulos et al., 1981; Holley et al., 1988b).
the pH value, can subsequently be used to adjust However, genuine salamis are made with little
the ripening climate so that the difference between sugar, allow only a moderate pH reduction and
the relative humidity in the chamber and the rela- are therefore traditionally ripened at lower tem-
tive humidity at the sausage surface is optimal for peratures. When such sausages were fermented at
the drying process. 23”C, addition of lactic acid bacteria (Lactobacil-
lus plan tarum, Lactobacillus sake, Lactobacillus
Improved control of pathogens curvatus or Pediococcus pentosaceus) markedly
contributed to the inhibition of S. aureus (Hechel-
Despite ail efforts by food hygienists, food-borne mann et al., 1988). This was due to a rapid de-
diseases are increasing rather than decreasing even crease of the pH to values below 5.3, and no
in countries with a large supply and variety of evidence for involvement of any other mechanism
cheap foods. Meat regularly contains pathogenic was found. At lower fermentation temperatures,
bacteria, and ingestion of fermented sausages has acid formation became less important. Initial a,
occasionally resulted in outbreaks of illness caused values below 0.955 even favoured S. aureus be-
by S. aureus and salmonellae. The control of these cause it slowed down acid formation. Nitrite had
pathogens in rapidly fermenting, smoked sausages only a minor inhibitory effect.
is well known (see Table 1 and the reviews cited in Salt and nitrite play an important role in sup
the Introduction). Later research (reviewed by pression of salmonellae early in the fermentation
Lticke & Earnshaw, 1991) has shown that for- when the pH is still above 5.3. Schillinger and
mulations and ripening parameters controlling Lticke (1989) found that sausages with only 2%
these bacteria are also inhibitory to other bacterial NaCl and 40-70 mg/kg sodium nitrite added
pathogens. On the other hand, there is an increas- (about half the usual amount) can be safely pro-
ing demand for more ‘natural’, less severely pro- duced if the pH is lowered to 5.3 within l-2 days
cessed meat products with no ‘chemical’ additives. at about 20°C. This, however, was only feasible
A crucial part in the development of new fermented with very rapid acid producers such as Lactobacil-
meat products and in the optimization of the manu- lus sake or by the use of acidulants such as glu-
facture of traditional products is the evaluation of cone-delta-lactone. Strains of lactic acid bacteria
the fate of pathogens. Research is focusing on the differed somewhat in their effect on salmonellae;
selection of lactic starter cultures which, ideally, these differences, however, were found to be
would kill rather than inhibit pathogens, and/or largely, if not entirely due to the formation of lac-
which could also be used as ‘biological preser- tic acids from fermentable sugars (glucose, glucose-
vatives’ for non-fermented meats. (j-phosphate, ribose) originally present in the meat.
Fermented meat products 305

Table 3. Components of aroma and tlavour of fermented microflora. The concentrations vary considerably
sausages (Vandekerckhove, 1977; Wortberg & Woller,
Compounds added as such:
1982). Recent work by Tschabrun et al. (1990) in-
- Salt dicated that the main cause of variation in the his-
- Spices tamine content was the age and microbiological
- Smoke constituents
quality of the raw material. However, further re-
Products of microbial degradation of carbohydrates: search is needed to minimize the amine content in
- Lactic acid
- Acetic acid
fermented sausages.
Products of protein degradation by microbial or meat enzymes:
- Amino acids Better flavour in less time
- Peptides
- Volatile fatty acids Lticke et al. (1990) collected the opinions of vari-
- Carbonyl compounds
ous experts from industry and research on desir-
Products of lipid degradation able improvements of sausage fermentation, with
- Medium- and long-chain fatty acids (formed by microbial
or meat lipases) special reference to starter cultures. Faster acid
- Carbonyl compounds (from hydroperoxides) formation ranked very low, and excessive acid
- Volatile fatty acids formation, often associated with colour defects,
- Hydrocarbons
sometimes also with gas formation, appears to be
Transformation products from additives (e.g. smoke or spice the main defect of fermented sausages in virtually
constituents)
all countries. Priority was given to the acceleration
of the formation of the curing colour, aroma and
Growth potential of Listeria monocytogenes flavour, and to the extension of the shelf-life of
during sausage fermentation is small, and condi- the product by delaying oxidative rancidity. Ac-
tions controlling salmonellae and S. aureus will cordingly, research towards a better understand-
also control this pathogen. However, L. monocyto- ing of aroma and flavour formation, particularly
genes may survive quite well in dry sausages, and on the role of microorganisms, was advocated in
it would be desirable to have starter cultures various comments both from meat scientists and
killing rather than merely inhibiting this bac- from manufacturers of starter cultures. However,
terium, L. monocytogenes is sensitive to various the picture is extremely complex because microbial
bacteriocins formed by lactic acid bacteria, includ- enzymes, meat enzymes, and non-enzymatic reac-
ing some strains competitive in sausage fermenta- tions all contribute to the development of a ‘bal-
tion. Schillinger et al. (1991) tested the effect of a anced’ aroma and flavour (Table 3). In addition,
bacteriocin-producing Lactobacilh sake strain on different consumers prefer different flavours. Prac-
L. monocytogenes in raw sausage mixture. Com- tical experience shows that extensive ageing of
pared with its bacteriocin-negative variant, this slowly fermented sausages prepared with high-
strain gave reproducibly about one log unit lower quality, firm fatty tissue leads to products with
Listeriu counts at ‘normal initial pH (55-5.7) and superior aroma and flavour containing higher
a delay of growth of L. monocytogenes at high initial amounts of products of lipid and protein degrada-
pH (6.36.4). Similar results were obtained by Berry tion. It is also commonly observed that some
et al. (1990) studying the effect of bacteriocin-pro- metabolic activities of catalase-positive cocci are
ducing pediococci in summer sausage fermentation. beneficial to the sensory quality of fermented
However, the benefit of bacteriocinogenic strains or sausages, at least for the German, French or
bacteriocins in meat fermentations or meat preser- Mediterranean consumer. There is some evidence
vation is limited: bacteriocins may act against de- that Micrococcaceue, in addition to reducing ni-
sired lactic acid bacteria, they are slowly inactivated trate, protect the product from deleterious effects
by binding to meat phospholipids, and resistant of oxygen by means of their peroxide and hy-
mutants of target bacteria can easily be isolated. droperoxide degrading enzymes (Table 2; see
Lticke, 1985, for a review). However, they are un-
Suppression of amiple formation able to replace the antioxidative effect of nitrite or
to delay the development of oxidative rancidity in
The concentration of biogenic amines in fer- fermented sausages prepared without nitrite and
mented sausages tends to increase with ripening nitrate (Riidel, W. & Lticke, F.-K., unpublished).
time and the activity of the proteolytic surface It is still doubtful if and to what extent catalase-
306 Friedrich-Karl Liicke

positive cocci contribute to aroma formation by Intoxikationen nach Verzehr von Rohwurst und
lipolytic activity. The strains available as starter Rohschinken. Mittbl. Bundesanstalt Fleischforsch. Kulm-
bath, Heft 100, 795664.
cultures show little if any lipolytic action on pork Holley, R. A., Jui, P. Y., Wittmann, M. & Kwan, P. (1988~).
fat, and addition of a strongly lipolytic strain has Uberleben von Staphylococcus aureus and Salmonella ty-
little effect on the aroma and flavour of a mould- phimurium in Rohwtirsten aus mechanisch separiertem Htih-
nerlleisch. Fleischwirtsch., 68, 205-12, 215. (English version:
ripened or chorizo-type fermented sausage (Rode1 Proceedings, 32nd European Meeting of Meat Research
et al., 1989; Arboles & Julia, 1991). Workers, Ghent, August 24-29, 1986, Vol. II, paper 5:5).
Because few details are known on the biochemi- Holley, R. A., Lammerding, A. M. & Tittiger, F. (19886).
cal activities related to aroma and flavour devel- Microbiological safety of traditional and starter-mediated
processes for the manufacture of Italian dry sausage. Znt. J.
opment during sausage ripening, it is very tedious Food Microbial., 7, 49-62.
to optimize the ripening process and very difficult Katsaras, K. & Leistner, L. (1988). Topographie der Bakte-
to accelerate it without affecting the sensory qual- rien in der Rohwurst. Fleischwirtsch., 68, 1295-8.
Landvogt, A. & Fischer, A. (1990). Rohwurstreifung -
ity. Likewise, it is very tedious to screen large Gezielte Steuerung der Sauerungsleistung von Starterkul-
numbers of potential starter strains for producing turen. Fleischwirtsch., 70, 1134, 113640.
a desired aroma or delaying rancidity, let alone to Leistner, L. (1986a). Allgemeines tiber Rohwurst. Fleisch-
wirtsch., 66, 290-300.
‘engineer’ strains to produce good-tasting prod- Leistner, L. (19866). Schimmelpilz-gereifte Lebensmittel.
ucts within a minimum of time. Fleischwirtsch., 66, 168-73.
Leistner, L. & Bern, Z. (1970). Vorkommen und Bedeutung
von Hefen bei Pokelfleischwaren. Fleischwirtsch., 50, 350-l.
Leistner, L. & Lticke, F.-K. (1989). Bioprocessing of meats.
REFERENCES In Biotechnology and Food Processing, ed. S.-D. Kung, D.
D. Bills & R. Quatrano. Butterworths, Boston, pp. 273-86.
Adams, M. R. (1986). Fermented flesh foods. In Progress in Liepe, H.-U. (1983). Starter cultures in meat production. In
Industrial Microbiology, Vol. 23, ed. M. R. Adams. Else- Biotechnology, Vol. 5, ed. G. Reed. Verlag Chemie, Wein-
vier, Amsterdam, pp. 159-98. heim, pp. 400-24.
Arboles, J. & Julia, E. (1991). Aroma in cured meat products. Lticke, F.-K. (1985). Fermented sausages. In Microbiology of
In Advanced Biotechnology and the Genetic Manipulation of Fermented Foods, Vol. 2, ed. B. J. B. Wood: Elsevier Ap-
Microbial Cultures for Meat Processing. COMETT II, plied Science, London, pp. 41-83.
Course A, Valencia, 29-30 April 1991. Lticke, F.-K. & Earnshaw, R. (1991). Starter cultures. In
Bacus, J. (1984). Utilization of Microorganisms in Meat Pro- Food Preservatives, ed. N. S. Russell & G. W. Gould.
cessing. Research Studies Press, Letchworth, UK. Blackie, Glasgow, pp. 215-34.
Berry, E. D., Liewen, M. B., Mandigo, R. M. & Hutkins, Lticke, F.-K., Brtimmer, J.-M., Buckenhtiskes, H., Garrido
R. W. (1990). Inhibition of Listeria monocytogenes by Fernandez, A., Rodrigo, M. & Smith, J. E. (1990). Starter
bacteriocin-producing Pediococcus during manufacture of culture development. In Processing and Quafity of Foods.
fermented dry sausage. J. Food Protect., 53, 194-7. Vol. 2: Food Biotechnology: Avenues to Healthy and Nutri-
Campbell-Platt, G. (1987). Fermented Foods of the World - tious Products, ed. P. Zeuthen, J. C. Cheftel, C. Eriksson,
A Dictionary and Guide. Butterworths, London. T. R. Gormley, P. Linko & K. Paulus. Elsevier Applied
Comi, G. & Cantoni, C. (1980). I lieviti in insaccati crudi sta- Science, London, pp. 2.1 l-36.
gionati. Zndustrie Alimentari, 19, 85760. Marcy, J. A., Kraft, A. A., Olson, D. G., Walker, H. W. &
Dainty, R. H. (1986). Chemical changes associated with mi- Hotchkiss, D. K. (1985). Fate of Staphylococcus aureus
crobial growth on meat stored at chill temperatures. Pro- in reduced sodium fermented sausage. J. Food Sci., 50,
ceedings, 32nd European Meeting of Meat Research 31&20.
Workers, Vol. I. Ghent, 24-29 August, pp. 179-86. Meisel, C., Gehlen, K.-H., Fischer, A. & Hammes, W. P.
Delarras, C. & Laban, P. (1981). Distribution of the different (1989). Inhibition of the growth of Staphylococcus aureus
Staphylococcus species according to their meat and dairy in dry sausages by Lactobacillus curvatus, Micrococcus vari-
origin. Zbl. Bakt. Hyg. I Orig. B, 173, 471-7. ans and Debaryomyces hansenii. Food Biotechnol., 3,
Demeyer, D. I., Verplaetse, A. & Gistelinck, M. (1986). Fer- 145-68.
mentation of meat - an integrated process. Belgian J. Metaxopoulos, J., Genigeorgis, C., Fanelli, M. J., Franti, C.
Food Chem. Biotechnol., 41, 131-9. & Cosma, E. (1981). Production of Italian dry salami. I.
Fischer, U. & Schleifer, K.-H. (1980). Vorkommen von Initiation of staphylococcal growth in salami under com-
Staphylokokken und Mikrokokken in Rohwurst. Fleisch- mercial manufacturing conditions. J. Food Protect., 44,
wirtsch., 60, 1046-8, 1050. 347-52.
Genigeorgis, C. A. (1989). Present state of knowledge on Nes, I. & Skjelkvale, R. (1982). Effect of natural spices and
staphylococcal intoxication. Int. J. Food Microbial., 9, oleoresins on Lactobacillus plantarum in the fermentation
327-60. of dry sausage. J. Food Sci., 47, 1618-21, 1625.
Hammes, W. P. (1986). Starterkulturen fur die Fleisch- Rodel, W. (1986). Rohwurstreifung - Klima und andere
wirtschaft. Chemie Mikrobiol. Technol. d. Lebensm., 9, EinfluDgrbBen. Fleischerei, 37, 33@40.
131-43. Riidel, W. & Stiebing, A. (1987). Kontinuierliche Messung
Hammes, W. P., Bantleon, A. & Min, S. (1990). Lactic acid des Reifungsverlaufs von Rohwurst. Fleischwirtsch., 67,
bacteria in meat fermentation. FEMS Microbial. Rev., 87, 1202, 1204, 1206, 1208, 1211.
165-74. Riidel, W., Stiebing, A., Lticke, F.-K. & Schillinger, U.
Hechelmann, H., Locke, F.-K. & Schillinger, U. (1988). (1989). Entwicklung eines Standards fur die Herstellung von
Ursachen und Vermeidung von Staphylococcus aureus - Salami nach italienischer und franzosischer Art. Abschlz&
Fermented meat products 307

bericht, FV ‘Biokonservierung von Lebensmitteln ‘. Bunde- ergieeinsparung bei der Rohwurstreifung. Fleischwirtsch.,
sanstalt f. Fleischforschung, Kulmbach. 62, 1383-9.
Schillinger, U. & Liicke, F.-K. (1989). Inhibiting salmonellae Tschabrun, R., Sick, K., Bauer, F. & Kranner, P. (1990). Bil-
growth in fresh spreadable Mettwurst. Fleischwirtsch., 69, dung von Histamin in schnittfesten Rohwtirsten. Fleisch-
879-82 (German version: Fleischwirtsch., 68, 1056, 10614, wirtsch., 70, 448-52.
10667 (1988)). Vandekerckhove, P. (1977). Amines in dry fermented
Schillinger, U., Kaya, M. & Lticke, F.-K. (1991). Behaviour sausages. J. Food Sci., 42, 283-5.
of Listeria monocytogenes in meat and its control by a bac- van Hoye, S. & Demeyer, D. (1987). Sausage metabolism as
teriocin-producing strain of Lactobacillus sake. J. Appl. affected by oxygen consumption and sausage diameter.
Bacterial., 70, 473-8. Mededehngen van de Faculteit Landbouwwetenschappen,
Seager, M. S., Banks, J. G., Blackburn, C. de W. & Board, Rijsuniversiteit Gent, 52, 1549-52.
R. G. (1986). A taaonomic study of Staphylococcus spp. Wirth, F. (1988). Kochsalzverminderung bei Fleischerzeugnis-
isolated from fermented sausages. J. Food Sci., 51, 295-7. sen - Miiglichkeiten und Grenzen. Fleischwirtsch., 68,
Selgas, M. D., Ordonez, J. A. & Sanz, B. (1988). Selected 947-52.
characteristics of micrococci isolated from Spanish dry fer- Wortberg, B. & Woller, R. (1982). Qualitat und Frische von
mented sausages. Faod Microbial., 5, 185-93. Fleisch im Hinblick auf ihren Gehalt an biogenen Aminen.
Stiebing, A. & Rodel, W. (1989). Kontinuierliches Messen der Fleischwirtsch., 62, 1457-60, 1463.
Oberflachen-Wasseraktivitat von Rohwurst. Mittbl. Bun- Zaika, L. L. & Kissinger, J. C. (1984). Fermentation en-
desanstalt Fleischforsch. Kulmbach, 28, 221-7. hanced by spices: Identification of active component. J.
Stiebing, A., Rodel, W. & Klettner, P.-G. (1982). En- Food Sci., 49, 5-9.

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