Meat Science, Vol. 49, No. Suppl.

I, Sl69--Sl77, 1998
0 1998 Elsevier Science Ltd
All rights reserved. Printed in Great Britain
PII: SO309-1740(98)00082-5 0309-1740/98/$19.00+0.00
ELSEVIER

Dry Fermented Sausages

K. Incze
Hungarian Meat Research Institute, 1097 Budapest, Gubacsi tit 6/b., Hungary

ABSTRACT

Two major aspects offermented sausages are discussed in the article. After a brief history
of enterohemorrhagic Escherichia coli with special regard to fermented meat products the
basic experimental designs and results are tackled on the basis of which safety issue in this
respect is thoroughly discussed. The results show a rather limited opportunity for meeting
food safety requirements with short or medium time ripened raw fermented sausages while
traditionally, long ripened sausages are in a much better position. Fermented meat pro-
ducts as probiotics are also discussed. After evolving the EHEC outbreaks caused by fer-
mented sausages the possibilities for jinding reliable methods and products have been
narrowed and more research is needed toJind optimum solution. c:, 1998 Elsevier Science
Ltd. AN rights reserved

INTRODUCTION

Fermentation and drying of meat products are probably the most ancient ways of pre-
servation under normal climatic conditions and in some cases under hot climate, too.
After gathering experience of some thousand years and after several decades of inten-
sive research in the field of fermentation and drying of meat products, manufacturing of
fermented meat products still ‘involves a lot of science, a little art and a certain amount of
mistique’ (Hand, 1997). From the 1950s on a real breakthrough in manufacturing of fer-
mented meat products can be observed: thanks to the research of Niinivaara and Niven
use of pure bacterial cultures in fermented meat products has been launched. This process
was a ‘triumphal march’ characterized by mutual utilization of knowledge of experts in
practice and in research. In some decades the new technology with application of starter
cultures gained an overwhelming victory: manufacturing of traditional dry sausages has
been changed not only ‘inside’ by addition of acidifying and aroma forming, nitrate
reducing starter cultures but also ‘outside’ using mould starters. The new technology
pushed gradually into the background those manufacturing practices where no starters
have been applied, claiming rightly the higher level of safety in case of starter application,
at least with sausages of short ripening time.
This almost idealistic situation lasted until such micro-organisms emerged or ‘devel-
oped’ that were less sensitive to the inhibiting factors produced by starter cultures and by
drying. While growth of salmonellae is inhibited by lower pH, lower temperature and
lower water activity and staphylococci are retarded in their growth by lower pH and
lower temperature, listeriae grow almost undisturbed at lower temperatures and lower

S169
s170 K. Incze

pH-values and EHEC (enterohemorrhagic E. coli) strains survive for a long time these
inhibiting factors that destroy many other micro-organisms.
Out of the almost innumerable interesting topics related to dry fermented sausages only
some will be dealt with in this review, such as safety issues with special regard to EHEC
strains and fermented sausages as probiotics.

ESCHERICHIA COLI IN DRY FERMENTED SAUSAGES

Eschericfzia coli, just as other Gram negative members of Enterobacteriaceae, has not
exhibited earlier a real problem with dry fermented sausages, unless serious mistakes of
hygienic and/or of technological nature have been made.
These microbes, being common contaminants of food raw material, usually disappear
from the fermented sausages as a result of the combined effect of low pH, low temperature
and low water activity. This effect is enhanced to some extent by the presence of nitrite
and also by other metabolites in addition to lactic acid produced by starter cultures. As a
consequence no E. coli could be found in a sausage fermented and dried according to
good manufacturing practice and there was no risk of recontamination and growth of E.
coli on dry sausages because of the inhibiting factors listed above. These factors have been
effective against other undesired bacteria as well: a sound basis for the firm belief that
fermented dry sausages have an excellent safety record. This was the situation until 1994
when an E. coli 0157:H7 outbreak was linked to presliced dry fermented salami in the
United States (Anon, 199%; Tilden et al., 1996) which was followed by an outbreak in
Australia linked to mettwurst, an uncooked semi-dry fermented sausage (Anon, 19953).
Even though dry sausage as vehicle of enterohemorrhagic E. coli is far less frequent than
either hamburger or other foods of animal and plant origin that are not or not sufficiently
heated, the excitement and perhaps too extreme reaction of health authorities seem justi-
fied for three reasons:

l the increasing number of E. coli 0157:H7 outbreaks and the severe consequences of
even low bacterial numbers,
l to learn that a product of excellent safety record can be a time bomb threatening
consumers with serious illness or even with death is a shocking new experience,
l the easy solution of the problem with other foods (‘they have to be cooked’) is not
really a solution with raw sausage.

BRIEF HISTORY

Some strains of E. coli, a species used earlier as a non-pathogenic indicator of enteric

pathogens, changed probably in the early 80s to virulent organisms represented by several
strains. These enterohemorrhagic E. coli (EHEC) strains acquired their Shiga or Shiga-
like toxin from Shigella. (E. coli strains acquired not only Shiga-like toxins but also other
virulence factors causing pathogenicity to humans or animals. In addition to EHEC also
enterotoxigenic /ETEC/, enteroinvasive (EIEC) enteroaggregative /EaggEC/, enter-
opathogenic /EPEC/ and diffusely adherent /DAEC/ strains are known. In this article
nevertheless only enterohemorrhagic E. coli will be discussed.) In 1982, two hemorrhagic
colitis (bloody diarrhea) outbreaks were observed where E. coli 0157:H7 was indentified
as causative agent and somewhat later the same micro-organism was found in feces of
children with hemolytic uremic syndrome (HUS) (Karmali et al., 1983; Riley et al., 1983).
HUS and other life-threatening complications like central nervous system deterioration,
 Dry fermented sausages s171

stroke, renal impairment and end-stage renal failure, etc., may occur in patients suffering
from hemorrhagic colitis (Buchanan and Doyle, 1997; Desmarchelier, 1997) the risk being
the highest with young children and with elderly people.
As a result of the dry sausage outbreaks in the United States (California and
Washington) the US Department of Agriculture and the Food Safety and Inspection
Service developed guidelines (Reed, 1995) that required fermented sausage manufacturers
to demonstrate a 5-log unit reduction in the enterohemorrhagic E. coli count during pro-
cessing (Hinkens et al., 1996). Since it was already known from earlier works (Buchanan
and Klawitter, 1992; Glass et al., 1992; Pozzi et al., 1996) that EHEC strains are rather
resistant to extrinsic and intrinsic factors, thus an easy solution for meeting the require-
ments of USDA Food Safety and Inspection Service was not foreseen.
First at University of Wisconsin a research project was launched sponsored by the
National Cattlemen’s Beef Association where raw meat batter was inoculated with a five-
strain E. coli 0157:H7 cocktail at levels of at least lo7 CFU g-i, the experiments were run
in triplicate. Acid and heat sensitivity of the strains were tested, (Freeman, 1996) and since
sausages were dried to different moisture:protein ratios also the effect of a, was con-
sidered indirectly. On the basis of the results five options have been worked out and sug-
gested, respectively.

Option 1: heat process, 63°C for 4 min

Option 2: companies develop and validate their inactivation treatment
Option 3: hold-and-test program for finished product (sub-samples from 15-30
individual chubs)
Option 4: combined treatments
Option 5: HACCP system including raw batter testing and a 2-log inactivation in
fermentation and drying

Food Safety and Inspection Service insists options 14 result in a five-log reduction of E.
coli 0157:H7.
Following the publication of these options research work on the fate of enterohemor-
rhagic E. coli influenced by factors common during fermentation and drying of sausages,
as well as on possible elimination of EHEC strains has been intensified.
It was already known that EHEC strains can be more tolerant to environmental fac-
tors, they have a high acid tolerance, surviving 2-7hr exposures to pH 2.5 and 37°C
(Benjamin and Datta, 1995; Buchanan and Edelson, 1996) and their salt tolerance can
also be remarkable compared to generic E. coli strains. There exist of course acid-tolerant
non-enterohemorrhagic and acid-intolerant enterohemorrhagic E. coli strains, too
(Buchanan and Doyle, 1997), but for safety reasons, chances of survival of more resistant
strains have to be considered and challenged in ‘five-log reduction’ studies.
A real limiting factor in finding EHEC-inactivating methods of technology is the fact
that intensifying almost any inhibitory effect of common dry sausage fermentation prac-
tice will alter palatability adversely, not to mention cooking that seems almost the only
effective means of 5-log reduction, yet very atypical method with a group of traditionally
raw products.

EFFECT OF FERMENTATION ON EHEC SURVIVAL IN MEAT

ENVIRONMENT

Experimental designs are usually similar in using a ‘cocktail’ of EHEC strains isolated
from outbreaks for inoculation studies but inoculation has not always been done in form
S172 K. hcze

of mixing in the batter (Hinkens et al., 1996; Yu and Chou, 1996; Calicioglu et al., 1997;
Gareis, 1997), injection of stuffed sausage was also used (Nissen et al., 1997) or inocula-
tion of slices of ready dry sausage was applied, too (Zeuthen et al., 1997).
In two similar experiments (Hinkens et al., 1996; Calicioglu et al., 1997) pepperoni and
all-beef summer sausage batter resp. were inoculated with a commercial Pediococcus
starter culture and a five-strain mixture of E. coli 0157:H7 (2 lo7 CFU g-i). The sausages
were fermented to pH 4.6 or 5.0 and then heated to different temperatures for different
periods. The results can be summed up as follows. Regardless of the final pH fermentation
alone resulted in only a l-2-1.39-log CFUg-’ decrease in EHEC number and no further
change could be observed after drying to a moisture: protein ratio of <1.6:1 either.
Heating on the other hand resulted in a definite lethal effect the extent of which was
influenced by final pH. Pathogen number was decreased by 27 log units in chubs of pH
4.6 after heating to an internal temperature of 54°C instantaneous but this decrease
reached only a 3.2~log unit with the same heating if final pH was 5.0. When holding these
sausages at 54°C for 30 or 60min, pathogen numbers decreased by 5-7 log units, respec-
tively. In pepperoni heating to internal temperatures of 53°C for 60min resulted in a 5-6
log unit reduction while heating to 63°C instantaneously ended up with a 27 log unit
decrease in number of pathogens.
Yu and Chou (1996) inoculated Chinese-style sausage batter with four strains of E. coli
0157:H7 and dried in 50°C air-blast drier for 6 hr, taking samples every 2 hr. They found
2-log unit reduction in pathogen number by the end of drying, when internal temperature
reached 48°C if sausage contained curing agents (a mixture of 13 additives including
sucrose, salt, nitrite, sorbate and ascorbate). Without curing mixture no reduction occur-
red. In tryptic soy broth with curing agents 6-log reduction in 4 hr and without curing
agents about 2-log unit reduction in 6 hr occurred with the same heating.
Nissen et al. (1997) inoculated freshly stuffed sausage (with Lactobacillus starter) with
low (103-1) and high (105p7) numbers of E. coli 0157:H7, Salmonella kentucky and Lis-
teria monocytogenes. The sausages were fermented and dried according to common
Norwegian practice and stored afterwards until 5.5 months at 4 and 20°C. In the low
inoculum samples E. coli number increased in the first few days of fermentation but then
decreased and no E. coli could be detected at the end of the storage period of 5.5 months
regardless of the storage temperature. In case of high inoculum samples E. coli number
decreased throughout the fermentation and drying period, yet they were undetectable at
the end of storage of 5.5 months only if the chubs were kept at 20°C. In the sausages
stored at 4°C about 5 x lo2 CFU E. coli per sample were found at the end of storage.
Water activity values were 0.91 (4°C) and 0.89 (2o”C), respectively, pH values 4.8 and 5.1.
Zeuthen et al. (1997) sliced Danish fermented sausage ready for sale and inoculated
with E. coli 0157:H7 in two batches, with 4 and with 400cellsg-’ sausage. The pH value
was 4.54 at the time of inoculation. Inoculated slices were vacuumpackaged and stored at
ambient temperature. After 7 days storage no survival of pathogens was detected in an
environment of 4.5 NaCl, 25.8% moisture and pH 4.5 with predominant growth of lac-
tobacilli.
Duffy et al. (1996) investigated the effect of pH, sodium nitrite and NaCl as well as heat
treatments of different intensity on the survival of E. coli 0157:H7 in fermented sausage.
Their findings were as follows: under extreme circumstances (pH 4.4; 4.8% salt;
300 mg kg-’ NaN02) a 4-log unit decrease in E. coli number could be detected, but the
growth of starter culture was inhibited, too, consequently no fermentation in pepperoni
occurred. With lowered salt concentration a reduction in E. coli number of approx. 2-log
unit was found, an increase of about 0.5-log unit compared with the standard process. A
further reduction in the number of E. coli, meeting the 5-log reduction requirement, could
be achieved only by a mild heating at 55°C for 1 hr.
 Dry fermented sausages s173

FERMENTED SAUSAGES AS PROBIOTICS

In the intestines of humans about one third of the faecal mass is made up by live bacteria
known as intestinal flora. Its beneficial and harmful fractions are well balanced in healthy
humans and the beneficial bacteria dominate. In gastro-intestinal disorders harmful bac-
teria outgrow beneficial ones, but if harmful bacteria dominate the detrimental effect is
not necessarily immediate, serious consequences may occur delayed (Mitsuoka, 1996).
Therapeutic use of lactic acid bacteria as an aid to cure some types of gastro-intestinal
disorders has been supported for almost a century (Cohendy, 1906; Hawley et af., 1959).
Ever since gets this topic intensive publicity, owing to other beneficial effect of lactic acid
bacteria, yet pros and cons are equally represented.
The early works started with soured milk: yoghurt, koumis and kefir were used for
medical purposes in Europe and in Asia long before the microbes responsible for the
favourable effect were recognized and identified (Hawley et al., 1959). Metchnikoff (1910)
attributed senility and arterio-sclerosis to toxins produced in the intestines because of
putrefaction, that can be cured by ingestion of large amounts of milk soured with Bacillus
bulgaricus.
Rettger et al. (1935) summarized more than 60 years ago the conditions on which the
success of lactobacillus therapy depends. They showed that it is necessary to use an
intestinal strain (L. acidophilus) in form of large number of viable cells. These criteria are
still valid and have been completed with some others since then. Whether administration
of lactic acid bacteria, even in large number, has really an unequivocally beneficial effect
on the health status is judged still contradictory. In the scientific literature one can find
optimistic and guarded opinions equally (Sanders, 1993). Latter claim that the mechanism
is still insufficiently known, and more research has to be done concerning antimicrobial,
anticholesteremic and anticarcinogenic effect of bifidobacteria (Driessen and de Boer,
1989; Tannock, 1990; Kurmann and Rasic, 1991). Sanders considers a further problem in
most cases the lack of direct evidence for a positive effect of lactic cultures on human
health, since many papers deal with experiments on animals, in vitro or on humans with
few subjects.
The questions whether the application of probiotic bacteria will bring the expected
health benefit and what factors are necessary to be considered are manifold:

- apathogenicity
- viable number and viability of the micro-organism
- natural habitat of the organism
- adherence of the probiotic culture
- acid and bile tolerance of the micro-organism
- extent of pathogen inhibition
- action as a potential immunogenic factor
- fermenting ability
- good flavor formation in the lactic food

It is evident that viable lactic acid bacteria in large number have to be administered if it
is aimed at reasonably high number in the intestine that can compete other microbes
already well adapted. In recent investigations strains selected for application in probiotics
are tested also for pathogen inhibition and adhesion to intestinal human cell linings
(Mogensen and Friis, 1997). Testing of all the properties listed above is advisable if we
want the probiotics do their duty (Velazquez and Feirtag, 1997). The detrimental effects of
gastric fluid on probiotic bacteria can be hampered when these microbes are consumed with
food, because this way pH is raised. It has been suggested that adherence and colonization
s174 K. Incze

can take place or at least has greater chance if to a human subject his own bifidobacteria
has been administered. It is interesting to note that even if the administered bifidobacteria
survive the effect of gastric juice and bile effect and have good adherence ability they may
not necessarily colonize the colon (Bouhnik et al., 1992), yet their transient presence and
their significant biochemical influences in vivo can exert the beneficial effect expected
(Savage, 1977). Whether this favorable effect comes from production of acid, bacteriocin,
some other factors or from their combination is not clear. Bacteriocins have usually a
narrow spectrum of inhibition, mostly against closely related bacteria (other lactobacilli).
For this reason selection of probiotic strains for bacteriocin production and their appli-
cation can have a negative effect by inhibiting or displacing native ‘desired’ lactobacilli,
not pathogens or putrefactives in the gastrointestinal system (Sanders, 1993).

DISCUSSION

Considering the resistance of EHEC strains to low pH and relatively low water activity as
well as the fact that the presence of 10-100 bacteria can cause serious illness the challenge
seems to be great and the real solution somewhat remote for several reasons:

l It is evident from the experimental data, that manufacturing of fermented sausages

according to common practice with some weeks ripening time will bring about only
l-2 log unit reduction in number of the pathogen, a value far less than required by
USDA-FSIS.
l Changing common practice to the extreme (lowering pH, raising salt and nitrite)
results in somewhat higher reduction of the pathogen but the product is of dubious
value from sensory point of view.
l Most of the experimental data suggest that heating is the only effective and reliable
method for a 5-log reduction in number of enterohemorrhagic coli. The question is
then: can these sausages be considered as raw fermented products? To what extent
will be the aroma affected adversely?
l Even if meat industry does its utmost for supplying consumers with safe products,
they still can run the risk of EHEC infection if fermented sausages are sliced at retail
outlets or at home inadvertently: an action well beyond the responsibility of manu-
facturer.

What solution seems then acceptable?

With short ripened products, if USDA-FSIS requirements have to be met, heating is

probably the only choice. It can not be excluded of course that multi-target preservation
and metabolic exhaustion (Leistner, 1995) will help in solving this problem, promising
results are shown by Nissen et al. (1997) and Yu and Chou (1996) in this respect, yet more
extensive research has to be done in order to meet safety requirements. Fashionable field
of research on bacteriocins (De Vuyst and Vandamme, 1994; Samelis et al., 1994) may
also contribute offering effective alternatives. With sausages of longer ripening period
option 5 (HACCP system including raw batter testing and a 2-log inactivation in fer-
menting and drying) seems an adequate solution.
Traditional, long ripened and dried sausages and salamis represent a special group of
products not only in terms of technology, pH value and richness in flavor and aroma
(Incze, 1987; Nagy et al., 1988; Incze, 1992), but also regarding the low risk as vehicle of
EHEC infection. If these products are heavily contaminated during slicing operations,
they can cause illness, just as any other food. If on the other hand the sausage batter is
 Dry fermented sausages s175

contaminated with enterohemorrhagic E. coli, that can occur also in case of GMP, they
most likely die off during ripening and drying, hardly influenced by pH-changes typical to
these group of products. According to the results of Gareis (1997) EHEC strains are
rather resistant to pH-values common with dry sausages, nevertheless decrease in a,-
values do have a lethal effect on these organisms, mainly if the effect is long lasting.
Keeping in mind the results of Nissen et al. (1997) where they stated that longer time and
relatively high temperature favours the destroying effect, we can expect an adequate safety
with traditionally dried sausages also with respect to enterohemorrhagic E. coli, since all
these factors are available during manufacturing and storage.
Traditionally manufactured and dried sausage with long ripening time is thus a group
of products that can be characterised not only by its unique flavor, aroma and stability
but also by its safety and these products will most likely have a fairly promising future,
too.
As for fermented sausages as probiotics several possible advantages as well as further
research need have been listed in this article. The future looked very promising, since
apathogenic micro-organisms of intestinal origin with good starterculture abilities have
been successfully isolated (Arihara et al., 1996, 1997) and tested experimentally. With the
emerging of EHEC nevertheless a real, almost unsurmountable problem has arisen. It has
been shown that in general probiotics can be applied with expected effect only if micro-
organisms are administered in large number and with high viability. Considering the
potential risk of EHEC infection, and fulfilling the requirement of USDA-FSIS the pos-
sible choices are as follows:

l heating the sausage which then will not be suitable as probiotics

l drying the sausage according to ‘good old’ traditions in case of which micro-organ-
isms in question are most likely inactive
l trying to meet Option 5 and hoping (evidently supported by research) that in this
case all the requirements concerning food safety, sensory value and effectivity of
probiotics will equally be fulfilled.

As a conclusion, we might say that if somebody has the intention to find the way of
elaborating a probiotic in form of fermented sausage, he must be aware of stepping on a
narrow path which is rough and needs a good piece of research and ingenuity in order to
reach the goal.

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