Hindawi

International Journal of Food Science

Volume 2021, Article ID 6696856, 15 pages
https://doi.org/10.1155/2021/6696856

Review Article
Indigenous Microbiota to Leverage Traditional Dry
Sausage Production

Noelia Zulema Palavecino Prpich ,1,2 Germán Edgardo Camprubí ,3 María Elisa Cayré ,1
and Marcela Paola Castro 1,2
1
Laboratorio de Microbiología de Alimentos, Universidad Nacional del Chaco Austral (UNCAus), Comandante Fernández 755,
Presidencia Roque Sáenz Peña, 3700 Chaco, Argentina
2
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), C1425FQB Buenos Aires, Argentina
3
Facultad de Ingeniería, Universidad Nacional del Nordeste (UNNE), Las Heras 727, Resistencia, 3500 Chaco, Argentina

Correspondence should be addressed to Noelia Zulema Palavecino Prpich; noe@uncaus.edu.ar

Received 30 December 2020; Accepted 19 January 2021; Published 31 January 2021

Academic Editor: James Owusu-Kwarteng

Copyright © 2021 Noelia Zulema Palavecino Prpich et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.

The main issue addressed in this review is the need for innovation in the artisanal production of dry fermented
sausages—leveraging rather than discarding tradition, together with some practical strategies available to achieve it. Throughout
the text, emphasis is placed on the autochthonous microbiota responsible for the identity and unique sensory characteristics of these
products. The available strategies to introduce innovation in this manufacturing process rely on metabolic flexibility of microbial
strains. In this sense, this review evaluates the application of several tools aimed at improving the quality and safety of artisanal dry
fermented sausages focusing on the microbial community role. The most studied alternatives to enhance dry sausage production
comprise the use of autochthonous starter cultures—including functional and/or probiotic strains, the production of bacteriocins,
and the generation of bioactive peptides, which have been thoroughly covered herein. The purpose of this work is to review recent
research about novel different strategies available for food technologists to improve safety and quality in the manufacture of dry
fermented sausages. Additional support strategies—quality product registers and innovation through tradition—have been
suggested as complementary actions towards a successful introduction of indigenous microbial communities into traditional dry
sausage production.

1. Introduction fermented sausages can be defined as meat products that

comprise a stuffed mixture of pork and/or beef, fat, salt,
Fermented meat products have been consumed for centuries and nitrate and/or nitrite, including eventually sugar and
throughout the world and constitute one of the most impor- different spices. Albeit less frequently, formulations can
tant types of food [1]. Their tradition has originated in the include poultry, lamb, goat, horse, camel, ostrich, and game
Mediterranean countries during Roman times [2], and their meats [5–9].
production was later extended to Germany, Hungary, and In Europe, fermented sausages can be divided into
other countries, including the United States, Argentina, and Northern and Mediterranean types [10]. Northern products
Australia [3, 4]. There is a wide variety of dry fermented are generally semidry sausages with pH below 5, while Med-
products on the global market as a consequence of variations iterranean products are dry sausages with long ripening and
in the raw materials, formulations, and manufacturing pro- drying processes,and pH values of 5.3–6.2 [4]. On the other
cesses, which come from the habits and customs of the differ- hand, traditional sausages found in the American market
ent countries and regions. They are closely connected to the are semidry sausages, fermented rapidly at relatively high
culture, heritage, and local identity of a given population, temperatures, with a short drying period leading to pH values
having a strong symbolic value. Regardless of their origin, below 5 and very different organoleptic characteristics [4].
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2 International Journal of Food Science

Latin American countries also produce fermented sausages; The extraction of certain meat proteins by salt, leading to the
their manufacture has a long history in Argentina, Brazil, emulsification of fat globules, depends on the bacterial acidifi-
and Uruguay, mainly due to Spanish and Italian traditions, cation process that causes protein denaturation; consequently,
as well as to the quality and availability of beef meat. Asian variations in salt or fat concentrations would concomitantly
and African countries also provide different types of fermen- affect microbial interactions within the meat matrix.
ted sausages, with ingredients and procedures that differ In addition, several technological innovations are being
substantially with those described above [11]. introduced into what are considered traditional meats. These
The stability of fermented meat products is mainly deter- innovations are meant to reduce production time, energy,
mined by acidification—brought about by lactic acid bacter- waste, and costs as well as to meet standards of production
ia—and water activity (aw ) reduction in the course of curing and safety [15]. Raising the standards of local products
and drying. In addition, biochemical and physicochemical entails quality improvement. It is noteworthy that quality is
changes occur as a result of the interactions among microor- a complex concept not only based on sensory properties
ganisms, meat, fat, and processing technology; the combined but also on less tangible factors, such as “traditional” and
effect of these factors is what produces the wide range of avail- “natural” characteristics. Innovations based on the reemer-
able fermented sausages. The development of the characteristic gence of tradition require quality guarantees and careful
flavor, aroma, and texture relies on biochemical and physico- labelling and contribute thereby to meet legal requirements,
chemical reactions in which several types of bacteria, yeast, to indicate differentiation, and to orientate and reassure
and fungi species interact within the meat matrix and its sur- consumers.
face. Lactic acid bacteria (LAB) and coagulase-negative cocci
(CNC)—including both micrococci and coagulase-negative 2. Indigenous Microbiota and Starter Cultures
staphylococci (CNS)—are the most predominant groups in
meat spontaneous fermentation [12]. Besides, filamentous In traditional sausages, the fermentation is known to rely on
fungi and yeasts exert a protective-like effect due to the forma- natural contamination by environmental microbiota occur-
tion of a superficial film preventing from excessive dehydration ring during slaughtering and manufacturing, being the spe-
and oxidation of the lipid fraction due to oxygen and light [13]. cific composition of the “house microbiota” responsible for
Small-scale facilities persist on traditional production the distinctive qualities of artisanal products from small-
methods where spontaneous fermentation is the leading pro- scale facilities [18, 19]. Although this autochthonous micro-
cess. When fermentation depends on the in-house flora, micro- biota plays a major role on flavor, texture, quality, and safety
organisms come from the meat itself and the surrounding of the final product, the high variability in bacterial amount
environment supplying particular—yet heterogeneous—char- and species may induce quality problems due to lack of nor-
acteristics to the product. Industrial development has led to malization and/or homogenization.
the use of commercial starter cultures to standardize and con- Consequently, the introduction of starter cultures in the
trol sausage manufacturing; however, these cultures are not manufacture of fermented meat products turns into a neces-
always able to reproduce especial flavors and features of arti- sary implementation in order to guarantee food safety and to
sanal dry sausages. A half-way between standardization and standardize the final product attributes [20]. Commercial
traditional methods could be the introduction of starter cul- starter cultures do not offer much flexibility for product dif-
tures especially designed using autochthonous strains isolated ferentiation [21] and are not always able to compete well with
from the facilities [14]. the house flora colonizing meat plants, whereby their use
Artisanal and traditional products have grown in popu- often results in losses of desirable sensory characteristics
larity, with a return to food consumption with local identity [22]. A culture that performs well in one type of fermented
[15]. Traditional products became more attractive largely sausage is not necessarily efficient in another type. The use
because consumers considered them more “natural.” That of indigenous strains isolated from spontaneously fermented
perception gives the food an identity that, in turn, engenders meats could accentuate artisan-like flavors [21]. Therefore,
appropriate cultures have to be selected according to the spe-
a certain familiarity [16]. In this sense, traditional fermented
cific formulation of the batter and technology of fermenta-
dry sausages are closely connected to the culture, heritage,
tion since environmental factors will interact to select a
and local identity of a given population. They also have a
limited number of strains that are competitive enough to
strong symbolic value and contribute to the sustainability dominate the process. The most promising microorganisms
and development of rural areas [17]. Thus, this trend could for starter cultures are those selected from indigenous micro-
be used as a development strategy for regional economies. biota, which are competitive enough to dominate during fer-
Within the current global economic framework, the need mentation, well adapted to the particular product and to the
to add value to food products—while preserving authenticity specific production technology, and with high metabolic
and traditional features—is a must. Regarding dry fermented capacities which can beneficially affect product quality and
sausages, it involves not only those attributes related to their safety, preserving their typicity [23]. Autochthonous meat
general appearance and taste but also the ones pertaining to starter cultures mainly comprise lactic acid bacteria (LAB)
nutritional aspects. Nowadays, health-related issues are the and coagulase-negative cocci (CNC).
cornerstone of public concern about food. Consequently, salt
and fat reductions have also been reviewed in this study—- 2.1. Lactic Acid Bacteria. Lactic acid bacteria have a leading
outside the microbial scope—in order to attend this need. role in dry sausage manufacture by acid production and its
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International Journal of Food Science 3

concomitant pH decrease, affecting both technological prop- cus, S. pasteuri, S. sciuri, S. succinus, S. vitulinus, and S. war-
erties and microbial stability of the final product. The pH neri, depending on the type of product [21]. Kocuria (K.)
reduction leads to coagulation of fibrillar proteins, which species are ubiquitous and are highly adapted to the niche
improves the firmness and cohesiveness of final products, of meat fermentation; the species K. varians and K. kristinae
enabling slicing [24]; simultaneously, pH drop accelerates were mainly found in fermented sausage [13].
the ripening process, which positively affects the moisture
of fermented meat products. Along with the production of 2.3. Yeasts and Molds. The surface of fermented meat sau-
lactic acid, LAB have a specific enzymatic profile that impacts sages is colonized by several yeasts and molds. These micro-
the taste, aroma, and texture of meat products. They exert organisms can play an important role in the quality of the
lipolytic and proteolytic activity through the action of lipases products through the formation of a superficial film which
and proteases which hydrolyze lipids and peptide bonds in exerts a protective action against both excessive dehydration
proteins, respectively. Lipolysis contributes directly to the and the oxidation of the lipid fraction due to oxygen and light
typical sensory characteristics of fermented meat sausages [36, 37]. They participate in flavor and aroma development
while proteolysis enhances their texture and favors the drying due to the enzymatic activities of their lipases and proteinases
process [25]. Some meat LAB have been shown to possess [38, 39] and the stabilization of red color of fermented sau-
significant nitrate and nitrite reductase activity, even though sages as a result of oxygen depletion [40, 41]. In addition,
these activities are more intense in CNC than in LAB [26]. they may contribute to increased product safety by antago-
For further reading, Palavecino et al. [27] had extensively nistic activity against toxigenic molds [42].
reviewed LAB technological properties and safety features. Among yeast, there is a clear predominance of the Debar-
In keeping with the reclassification of lactobacilli pub- yomyces genus on a diverse group comprising Candida,
lished by Zheng et al. [28], LAB species mainly used as Yarrowia, Rhodotorula, Pichia, and Trichosporon [43, 44].
commercial starter cultures are Latilactobacillus (L.) sakei, Debaryomyces (D.) hansenii is the species most frequently
L. curvatus, Lactiplantibacillus (Lc.) plantarum, Lc. pentosus, and abundantly isolated [36, 39, 45]. The fungal population
Lacticaseibacillus (Lcc.) casei, Pediococcus (Pd.) pentosaceus, comprises mainly Penicillium and Aspergillus genera [46]
and Pd. acidilactici [26], while L. sakei, L. curvatus, and Lc. while other genera such as Mucor, Cladosporium, Scopular-
plantarum are the principal species of LAB usually found in iopsis, Geotrichum, and Alternaria have been found less fre-
spontaneously fermented sausages [29–31]. Members of quently. Penicillium is the most emblematic microbiota of
other LAB genera, such as Weissella, Leuconostoc, Lactococcus, fermented meat sausage surfaces [38], with the prevalence
and Pediococcus are generally found as minority species [12]. of Penicillium (P.) nalgiovense, followed by P. olsonii, P. chry-
sogenum, P. commune, P. solitum, and P. salamii [47].
2.2. Coagulase-Negative Cocci. The main technological func- Species such as D. hansenii, P. chrysogenum, and P. nal-
tion of CNC is their nitrate reductase activity exerting a defin- giovense are currently used as standard starter cultures. They
itive effect on typical color development and stabilization of help to improve and standardize the quality and safety of the
dry sausages. This enzymatic activity relies on the ability of final products [43, 46].
these cocci to reduce nitrate (NO3−) to nitrite (NO2−). Red col-
oration is formed in dry sausages by means of nitrite reduction 3. Strain Selection and Design of an Indigenous
that leads to nitric oxide (NO), which reacts with myoglobin to Starter Culture
form nitrosomyoglobin (MbFeIINO), the compound respon-
sible for the color [32]. Staphylococci can also synthesize nitric Native species that present attractive technological properties
oxide from arginine via nitric oxide synthase [33]. Proteolytic can be used to design autochthonous starter cultures that
and lipolytic activities are among the desirable metabolic char- ensure safety and quality of traditional products without
acteristics in CNC species [34, 35], releasing several com- altering their typicity. Thus, the introduction of an indige-
pounds that contribute to the characteristic flavor and nous starter culture into the production line constitutes an
texture of fermented meat products, i.e., peptides, amino acids, excellent example of the concept “innovation through tradi-
carbonyls, and volatile substances [34]. Despite being lipolysis tion” (ITT).
mostly performed by endogenous enzymes, CNC lipases can The first stage in the designing process of starter culture
be involved in this process and help to release fatty acids endogenous to small-scale facilities consists of isolating micro-
through incomplete β-oxidation. Besides, CNC enzymes are organisms from the niche in which the culture will subsequently
able to hydrolyze ester compounds; they also have catalase be applied. Strains should be selected from the pool of isolates
and superoxide dismutase activity which act as natural antiox- based on technological properties and safety characteristics.
idants providing safety [21]. Further technological and safety Once picked, these isolates should be genetically identified.
properties have been extensively described by Palavecino General technological properties of interest regarding BAL
et al. [27]. and CNC were summarized by [48], whereas selection criteria
Staphylococcus (S.) carnosus and S. xylosus are two CNC for yeasts and toxicologically safe molds can be found in the lit-
species commonly used as commercial starter cultures to erature [43, 46, 49]. Modern approaches for selection of the best
assist in color and flavor formation [23]. Many other CNC strain(s) for autochthonous starter cultures have integrated
species prevail in spontaneously fermented sausages, either technical, safety, and health-promoting features [25, 26, 50,
as dominant: S. xylosus, S. saprophyticus, and S. equorum, 51]. New molecular techniques introduced into the Food
or as subdominant: S. carnosus, S. epidermidis, S. haemolyti- Microbiology field complement the studies carried out so far
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4 International Journal of Food Science

and allow scientists to overcome the limitations of traditional An autochthonous starter culture that improves the
methods [13, 25]. Albeit these advances are helpful for the quality, safety, and homogeneity in traditional sausage
understanding of meat fermentation, these new technologies manufacture represents a beneficial tool to add value to these
are not easily accessible to researchers from emerging countries. products. For fermented foods, microorganisms that are con-
Several authors, around the world, have selected indige- sidered autochthonous are often associated with a given area
nous microbiota to apply as starter cultures in traditional and should be reported as a typical food ingredient. These
dry sausages; some examples are listed in Table 1. As shown microorganisms represent a direct link between food and his-
in the table, the species of microorganisms used in different torical and environmental conditions from their original
products are the same; however, the variability at strain level habitat [16]. Narratives about such quality-enhancing func-
is relevant. Therefore, a case-by-case evaluation of a potential tionalities are increasingly being used by starter culture pro-
bacterial strain to be used as a starter culture must be carried ducers, which promote self-styled cultures for “traditional”
out. Once microorganisms are selected, their compatibility meat fermentation [59, 60].
must be checked to determine whether their viability, meta-
bolic activities, and technological features are kept. The desir-
able scenario is the one where the selected microbes 4. Probiotics
contribute together to the final product without compromis-
ing any of their attributes or, even better, when they act addi- Over the recent decades, the meat industry has focused on
tively or synergistically [52, 53]. Furthermore, the selected enhancing potential health benefits of its products. In this
strains that comprise the designed starter culture should sense, the incorporation of probiotic cultures in traditional
improve the quality and safety whereas keeping or enhancing meat products could represent an alternative to improve
typical sensory attributes of regional products [20, 21, 50, 54]. their functional profile. The use of probiotic strains in associ-
ation with the traditional starter culture has been recognized
Hence, it is advisory to evaluate the sensory profile of the
as a technologically feasible and effective strategy for the
final products, being color, aroma, taste, texture, and overall
development of innovative products [61].
appearance, the attributes more frequently investigated [20,
Probiotic cultures are “live microorganisms that, when
53, 55]. Another important aspect to revise is the consistency
administered in adequate amounts, confer a health benefit
or robustness of the fermented sausages throughout different
on the host” [62] and comprise both bacteria and yeast.
production batches, i.e., along a year or a prolonged period, The main genus used as probiotic in meat products is
which could guarantee the homogeneity of the product and Lactobacillus, although other related genera have also been
a good performance of the starter culture [14]. Microbiological reported, such as Bifidobacterium, Enterococcus, and Pedio-
and physicochemical characteristics of the products must be coccus [63, 64]. Among yeasts, D. hansenii has been shown
monitored throughout the manufacturing process. Regarding to have probiotic traits, so it could be considered in future
the microbiological characteristics, changes in population innovative developments [65]. The probiotic mechanisms
dynamics and hygienic quality of the products at the end of are considered strain-specific and species-specific and some
the ripening stage must be monitored, according to the legisla- mechanisms might be widespread among commonly studied
tion established in each country or geographical area. Among probiotic genera [66].
the physicochemical parameters, pH and aw can be evaluated Fermented meat products are adequate for the carriage of
along the process, while salt content, color, texture, fatty acid probiotic bacteria since they do not undergo heat treatment,
profile, and volatile compounds can be determined in the final or else, it is very mild [26, 67]. In addition, it has been postu-
product [14, 20, 22, 53, 56, 57]. Even though these parameters lated that meat matrix protects the survival of probiotic lacto-
are indeed descriptive, a thorough assessment of the autoch- bacilli through the gastrointestinal tract [68]. However, the
thonous starter culture performance can only be achieved viability of probiotics can be affected by high content of cur-
when sensory attributes are also examined. ing salt, low pH, and low water activity of fermented meat
Ferrocino et al. [58] presented a novel work introducing an products. In this case, technologies such as microencapsula-
advance in the understanding of meat fermentation by coupling tion, which have demonstrated their potential to maintain
DNA sequencing metagenomics and metabolomics approaches probiotic viability during processing, storage, and passage
to describe the microbial function during this process. They through the gastrointestinal tract, can be used [69].
proved that a starter culture drastically affected the organoleptic Probiotic cultures in fermented sausages could be autoch-
properties of the products by the correlation between the vola- thonous bacteria with probiotic properties or commercial pro-
tilome profile, microbiota, gene content, and consumer accept- biotic strains with documented health-promoting properties.
ability. This evidence highlights the importance of selecting a In the first case, the potential probiotic strains can be obtained
starter culture to optimize production efficiency and product from fermented sausages by screening microorganisms that
quality. In addition, metagenomics can be a useful tool when possess appropriate physiological requirements and health-
it is integrated to metabolic and sensory analyses giving a better promoting properties [70–73]. Even though these potential
understanding of the functions of starter cultures in situ [25]. probiotic strains might be well adapted to the fermentation
These authors suggested that it might be probable—in the near meat niche, their benefits must be demonstrated in
future—to know which composition of starter cultures to use in randomized, controlled, or equivalent human trials, either in
certain technological conditions according to the sensory attri- a heterogeneous or stratified population (based on defined
butes desired for the product. characteristics of host or microbial genomics). Furthermore,
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International Journal of Food Science 5

Table 1: Indigenous starter cultures evaluated in the production of dry fermented sausages.

Product Strains or combinations of strains Inoculum (cfu/g) Processing place References

Traditional dry fermented L. sakei F08F202+S. equorum F08bF15+S. succinus 6 French traditional
1 × 10 [152]
sausage F08bF19 processing unit
L. sakei 8416
L. sakei 4413
Greek fermented sausage L. sakei 8426 2 – 5 × 107 N.E. [20]
Lc. plantarum 7423
L. curvatus 8427
Basilicata fermented
L. sakei DBPZ0062+S. equorum DBPZ0241 1 × 106 Artisanal industry [22]
sausage
Pd. acidilactici MC184+S. vitulinus RS34
Iberian dry fermented
Pd. acidilactici MS198+S. vitulinus RS34 5 × 107 Two different industries [153]
sausage
Pd. acidilactici MS200+S. vitulinus RS34
L. sakei LS131+S. equorum SA25
Galician chorizo L. sakei LS131+S. epidermidis SA49 1 × 106 – 107 N.E. [154]
L. sakei LS131+S. saprophyticus SB12
Slow dry-cured fermented D. hansenii M4+C-P-77S bactoferm1
1 × 106 N.E. [155]
sausages D. hansenii P2+C-P-77S bactoferm
Traditional dry sausage L. sakei 487+S. vitulinus C2
1 × 106 Small-scale facility [14, 53]
from Chaco L. sakei 442+S. xylosus C8
Chinese fermented dry Lc. plantarum CMRC6
1 × 107 Food pilot plant [128]
sausage L. sakei CMRC15
P. nalgiovense ITEM 15292+Startec TCSD12
1.48 log cfu/cm2
Salami P. salamii ITEM 15302+Startec TCSD1 (surface Two different industries [156]
1.93 log cfu/cm2
inoculation for fungi)
Lc. plantarum+S. xylosus
Fermented camel sausage 1 × 107 N.E. [125]
Lc. pentosus+S. xylosus
Horse meat sausage L. sakei 121 1:5 × 106 Small-scale facility [8]
(Lc. plantarum PC23+S. xylosus SA23)
Sardinian fermented 1 × 106
+D. hansenii Ca3 Farm scale [45]
sausages 5.9-8.3 log cfu/g
D. hansenii Ca3 (surface inoculation for yeast)
Chinese dry fermented Lc. plantarum R2
1 × 107 N.E. [157]
sausage Lc. plantarum R2+S. xylosus A2
1
C-P-77S bactoferm: starter culture containing Lc. pentosus and S. carnosus (Chr. Inc., Hansen, Denmark). 2Startec TCSD1: commercial starter culture, Tec-Al
S.R.L. N.E.: not specified.

dose and genome strain characterization should also be con- lus (Lm.) reuteri ATCC 55730 suffered from the harsh condi-
sidered [74]. tions of meat fermented matrix. Rubio et al. [79] found a
On the other hand, commercial probiotic strains and cul- good performance of the Lcc. rhamnosus CTC1679 strain,
tures isolated from human intestinal systems, with docu- isolated from the human intestine and with potential probi-
mented health-promoting properties, can be used [75]. In otic properties, in the manufacture of low-acid fermented
this case, the performance of these cultures in the fermenta- sausages “fuets.” Subsequent studies showed that Lcc.
tion niche should be evaluated [76]. Regardless of the origin rhamnosus CTC1679 colonized the gastrointestinal tract of
of the probiotic culture, it should not affect the sensory char- healthy volunteers, confirming that it could be delivered as
acteristics of the traditional product. a probiotic in fermented sausages [80]. Ayyash et al. [81]
In this sense, the potential use of lactobacillus strains evaluated Lc. plantarum KX881772, a new probiotic isolated
(Lcc. casei, Lcc. paracasei paracasei, Lcc. rhamnosus, and L. from camel milk, in semidry fermented camel sausages, find-
sakei sakei) isolated from a traditional Italian dry fermented ing that this probiotic has promising characteristics for the
sausage as probiotics was evaluated for Rebucci et al. [77]. meat industry.
Klingberg et al. [78] found that strains Lc. plantarum and Regarding microencapsulated probiotic microorganisms,
Lc. pentosus originated from fermented meat products were Muthukumarasamy and Holley [82] reported that Lm. reu-
in agreement with the definition of probiotics and their appli- teri ATCC 55730—encapsulated in sodium alginate—was
cation in the fermented sausages was a success without affect- used in fermented meat products. Technological characteris-
ing the flavor of the product. De Pisco and Mauriello [69] tics were not affected, and pH and aw values were similar in
reported that some probiotic strains such as Limosilactobacil- sausages with encapsulated probiotics and control sausages
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6 International Journal of Food Science

(free cells), while bacterial viability was also suitable. Sidira 5.1. Antimicrobial Compounds. The main antimicrobial effect
et al. [83] evaluated immobilized Lcc. casei ATCC 393 on responsible for safety of dry sausage is evidently the rate of
wheat grains in probiotic dry fermented sausages containing acidification of the raw meat [89]. Lactic acid bacteria present
reduced or negligible amounts of curing salts. Microbiologi- in the matrix can exert antagonism through competition for
cal and strain-specific multiplex PCR analyses confirmed nutrients and/or production of several antimicrobial sub-
the levels of Lcc. casei ATCC 393 in all samples after 71 days stances such as organic acids (lactic and acetic), carbon diox-
of ripening ranged above the minimum concentration to ren- ide, hydrogen peroxide, diacetyl, ethanol, and bacteriocins.
der a probiotic effect (6 log cfu/g). Ünal Turhan et al. [84] Production of bacteriocins during fermentation of meat plays
evaluated the production of sucuk with Lc. plantarum as an important role in enhancing the functional value of meat
starter culture, together with microencapsulated or free cells products, but production of other antimicrobial compounds
of Lcc. rhamnosus (probiotics strains). Textural, physicochem- by specific starter cultures can also be used in fermented
ical, and sensorial properties of sucuk with microencapsulated sausages.
microorganism were found to be similar to traditional sucuk. The role of bacteriocin-producing cultures used as starter
Recently, various studies showed strong evidence that cultures—or as adjunct cultures—is twofold: they can con-
bacterial viability is not an essential requirement to confer tribute to both flavor and food safety, providing fermentation
health benefits; hence, terms such as paraprobiotics and post- and preservation at the same time. As an illustration, there
biotics were created to denote health benefits beyond the are commercial cultures such as Bactoferm™ (Chr. Hansen,
inherent viability of probiotics. These terms represent new Denmark), containing pediocin-producing and sakacin-
categories of biological response modifier agents [85]. The producing strains, used in the manufacture of fermented sau-
scientific evidence supports that postbiotics and paraprobio- sages and dry-cured meat and Holdbac® protective cultures
tics possess diverse functional/bioactive properties such as (DuPont Nutrition and Biosciences, USA), containing a
antimicrobial, antioxidant, antihipertensive, and immuno- mix of bacteriocin-producing strains, used to protect meat,
modulatory activities, although mechanisms implicated in seafood, and dairy products from Listeria, yeasts, and molds
most bioactivities of postbiotics and paraprobiotics are not [90]. Beyond their role as biopreservatives, bacteriocins are
fully understood [66]. Fermented meat products could natu- gaining credibility as health modulators, due to their ability
rally contain postbiotics and paraprobiotics, but they cannot to regulate the gut microbiota, which is strongly associated
be controlled, and the amount produced may be insufficient with human wellbeing [91].
to generate a physiological response in vivo [86]. Several strains of L. sakei [70, 92], L. curvatus [93–96], Lc.
plantarum [97–99], and Pd. acidilactis [100] isolated from
5. Antimicrobial and Functional Metabolites traditional fermented sausages have been reported to pro-
duce different bacteriocins, among which curvacins and
New findings and sophisticated technology applied to the sakacins are the best known. These bacteriocins are of partic-
study of microbial metabolites have blurred the line between ular interest due to their high inhibitory activity against Lis-
several definitions. Among the most recent literature, the teria (Li.) monocytogenes even though other pathogenic and
abovementioned term “postbiotic” is still wide open, mainly spoilage microorganisms could also be affected. Extended
when it is referred to as an adjunct substance for food pro- data regarding the successful use of several bioprotective cul-
duction. According to Moradi et al. [87], any soluble factor tures used in fermented meat products can be found in
(products/metabolic by-products of microbial metabolisms Aymerich et al. [101] and Oliveira et al. [4].
or substances produced by the action of microorganisms on On the other hand, some authors have reported CNS
culture/food ingredients) secreted by food-grade microor- with antimicrobial activity in preliminary studies, although
ganisms, or released after cell lysis, during the growth and the bacteriocin production has been mainly described in
fermentation in complex microbiological cultures, food or LAB. In this sense, Lauková et al. [102] found that S. xylosus
gut, can be considered as such. In the light of this definition, SX S03 1M/1/2 produced a thermostable bacteriocin which
bioactive peptides, exopolysaccharides, bacteriocins, and could be used as starter culture or meat additive. Sánchez
organic acids could be ascribed to the term postbiotic. These Mainar et al. [103] reported that S. sciuri I20-1 exhibited
metabolites can exert some benefits to the food or host [88] activity against S. aureus and Clostridium (Cl.) botulinum,
and could add value to traditional fermented products, owing to the release of its bacteriocin-like substance in a meat
applied as an adjunct to living microorganisms—which play model system. The production of bacteriocins by potential
a technological role in the manufacture of these products—- CNS starter cultures to fight against S. aureus and Cl. botuli-
since postbiotics are more stable and safer for food applica- num in fermented meats could represent a complement to
tions than their producing microorganisms and their existing antilisterial LAB cultures for the production of safer
viability is not required either during consumption or pro- meat products, in particular when curing agent concentra-
duction [85]. tions are lowered [21].
The examples hereafter comprise the most studied bioac- The use of antagonic microorganisms isolated from tra-
tive metabolites in fermented meat products. Albeit these ditional meat products may be an important strategy to ade-
metabolites are currently generated in situ, this field could quately control toxigenic fungi and protect consumer health
be further expanded through the use of cell-free supernatant, from the hazard of exposure to mycotoxins such as ochra-
from the producing strains, as adjunct agents to indigenous toxin A (OTA), aflatoxins (AFs), and cyclopiazonic acid
starter cultures. (CPA) [42].
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International Journal of Food Science 7

Lactic acid bacteria produce several metabolites able to impact on body functions and may influence health. They
inhibit fungal growth, which can also participate in myco- are encrypted within the sequence of the parent protein and
toxin degradation and/or removal from contaminated food can be released through hydrolysis by proteolytic enzymes.
[104, 105]. Lactobacilli isolated from pork meat and salami In ripened foods, as dry fermented sausages, hydrolysis can
showed the ability to inhibit the growth of several molds be performed either by endogenous enzymes or by the com-
in vitro [106, 107]. Recently, Álvarez et al. [108] reported that bined action of endogenous and microbial enzymes [120].
Enterococcus (E.) faecium SE920, isolated from dry fermen- Health benefits of BP are continuously being explored and
ted sausages, could be a good candidate to reduce mycotoxin discovered; hence, there are still controversies regarding their
production in dry fermented sausages. In fact, the presence of magnitude and significance. Lafarga and Hayes [121] indi-
these strains significantly reduced OTA production of P. nor- cated that BP have antimicrobial, antioxidative, antithrom-
dicum in a dry fermented sausage-based medium under con- botic, antihypertensive, anticancerogenic, satiety-regulating,
ditions simulating sausage ripening. and immunomodulatory activities and may affect the cardio-
Antifungal activity was observed in CNS as well. Cebrián vascular, immune, nervous, and digestive systems. Peptides
et al. [109] reported that meat-borne S. xylosus Sx8 exhibited may also be effective in the treatment of mental health dis-
antifungal activity against toxigenic fungi such as P. eases, cancer, diabetes, and obesity. Furthermore, many
nordicum, Aspergillus (A.) flavus, A. parasiticus, and P. gri- known BP are multifunctional and can present two or more
seofulvum, triggering a significant decrease on mycotoxin health-promoting activities which may or may not be related
accumulation in ham-based medium. However, S. xylosus [122]. Antioxidant and antihypertensive peptides have been
Sx8 antifungal mechanism has not been elucidated yet. observed in meat products such as Spanish dry-cured ham
Among yeasts, D. hansenii is the most studied species as and dry fermented sausages [123, 124] and Tunisian dry
potential protective culture in fermented sausages because fermented camel sausages [125]. Throughout the manufactur-
of its predominance in these products [39, 43, 45]. This yeast ing process, LAB exert an exhaustive proteolysis on the meat
species has several mechanisms that can tackle fungal growth matrix. This proteolytic system comprises a cell wall-bound
and mycotoxin production in foods [65] and has been incor- proteinase, peptide transporters, and various intracellular
porated in the list of qualified presumption of safety (QPS) of peptidases, including endopeptidases, aminopeptidases, tri-
the European Food Safety Authority [110]. The use of peptidases, and dipeptidases [126], which contribute to the
autochthonous D. hansenii strains provided a positive contri- generation of small peptides and free amino acids [127].
bution to control the development of spontaneous mold pop- Although it is known that the degradation of main myofibril-
ulation on fermented Sardinian sausage surface [45] and lar and sarcoplasmic proteins took place in meat products
decrease the growth of ochratoxigenic P. verrucosum in dry [128, 129], peptides generated in dry fermented meat products
fermented sausage as a result of the combination of competi- have been less studied. Recently, a study from Mora et al. [124]
tion for space and nutrients and production of volatile com- reported that intense proteolysis occurred during processing
pounds [49]. In addition to the inhibition of the toxigenic due to the action of peptidases from muscle and LAB using a
mold growth, D. hansenii isolated from dry-cured meat has peptidomic approach.
also shown the ability to reduce OTA and AF content in Regarding what concerns this review, the use of autoch-
dry fermented sausages against P. verrucosum and A. parasi- thonous strains as potential bioactive peptide releasers has
ticus at transcriptional level [111, 112]. been assessed by few authors. Among three strains isolated
Competition for nutrients and space, together with the from a camel meat sausage obtained by fermentation with
production of peptides and proteins with antifungal proper- endogenous microflora, Mejri et al. [125] found that the batch
ties—including a group of small, basic, and cysteine-rich inoculated with S. xylosus and Lc. plantarum (107 cfu/g) had
antifungal proteins (AFPs)—is the main mechanism by higher antioxidant and antihypertensive capacities than the
which some nontoxigenic molds could collaborate in the noninoculated sausages. Fractions with molecular weights
control of undesirable fungi and improve product safety below 3 kDa showed the highest antioxidant and antihyper-
[113–115]. Penicillium chrysogenum isolated from dry- tensive capabilities in comparison with fractions above
cured meat [116] produces the antifungal protein PgAFP 3 kDa, which were observed at the end of ripening. Analysis
[117] and has shown potential as protective culture by inhi- of these fractions by RP-HPLC-ESI-Q-TOF-MS/MS allowed
bition of P. griseofulvum CPA production on dry fermented the identification of 13–22 peptides with a number of amino
sausage during ripening [118]. On the other hand, the anti- acids that ranged from 4 to 23. These peptides shared many
fungal protein PgAFP produced ex situ was effective in common features with other antioxidant and antihypertensive
reducing growth of toxigenic A. flavus and P. restrictum in peptides. Escudero et al. [123] and Mora et al. [124] stated that
dry fermented sausages, but its effect was time limited low molecular weight peptides (<3 kDa), contributing to the
[113]. However, Delgado et al. [119] indicated that the com- development of flavor in dry fermented meat products, could
bination of PgAFP and D. hansenii could be used as a preven- also exert antihypertensive activity.
tive measure against aflatoxigenic A. parasiticus or as a A study focused on health-promoting benefits of fermen-
corrective action when this mold has been detected in fer- ted camel sausages conducted by Ayyash et al. [81] showed
mented sausages. that the probiotic bacteria Lc. plantarum KX881772—iso-
lated from camel milk—played a promising role at imparting
5.2. Bioactive Peptides. Bioactive peptides (BP) have been functional characteristics to these sausages. The release of
defined as specific protein fragments that have a positive bioactive peptides with greater antioxidant capacities, ACE
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8 International Journal of Food Science

inhibition, and cytotoxicity (antitumoral) activity than the De Almeida et al. [138] evaluated the performance of
control was due to a high degree of hydrolysis achieved with autochthonous starter cultures in a low-sodium fermented
the addition of the probiotic strain to the camel sausage. sausage model, containing 1% NaCl, 0.25% KCl, and 0.25%
Fernández et al. [130] presented the joint use of an CaCl2. They found a combination of strains with peptido-
autochthonous starter culture composed by the strains Pd. genic potential (E. mundtii CRL35+S. vitulinus GV318) and
acidilactici MS200 and S. vitulus RS34, together with the pro- another combination with influence on the production of
tease EPg222 (purified from P. chrysogenum Pg222, which amino acids (L. sakei CRL1862+S. vitulinus GV318). This
was isolated from dry-cured meat products). Their study release of amino acids and small peptides is frequently related
showed that angiotensin-I-converting enzyme (ACE) inhibi- to the taste of processed meat.
tory and antioxidant compounds were released during the Dry fermented sausages are one of the most difficult meat
ripening process of dry fermented sausages. Even though products as far as fat reduction is concerned since excessive
the main proteolytic effect had been attributed to the enzyme, fat reduction leads to unacceptable appearance and undesir-
they suggested the combined use of the autochthonous able changes in texture [133]. While removing back fat from
starter and the enzyme since both had proved to give the best the batter is a simple way to perform this reformulation, lim-
organoleptic and hygienic profiles in previous studies [56]. itations are given by the reduction of sensory and technolog-
ical quality of product [76]. The replacement of animal fats
with plant oil sources in processed meat products affects
6. Reduction of Salt and Fat the drying process and presents problems such as inadequate
drying, binding, and retention of liquid oils [139, 140].
Sodium chloride is an important ingredient in processed Olivares et al. [141] reported that with a reduction of fat
meat due to its preservative properties, its capacity to affect in the raw material of around 15%, using controlled ripening
taste and improve product flavor, and its functional capacity conditions and slow fermentation process, they obtained fer-
to solubilize myofibrillar proteins, which is necessary in order mented sausages with high consumer acceptability. Then,
to enhance adhesion and cohesiveness in processed meat they studied the effect of fat content (10, 20, and 30%) and
products [131]. Granulated fat contributes to the continuous ripening time and found that fat reduction decreased lipoly-
release of moisture—a process necessary for the fermentation sis, lipid oxidation, and lipid-derived volatile compounds
and flavor development [132]. Fat contributes to the texture, during processing while the volatile compounds generated
mouthfeel, juiciness, and lubricity and constitutes a source of from bacterial metabolism increased, although only in the
essential fatty acids and fat soluble vitamins [133]. first stages of processing. The consumer preference in aroma
In recent years, increased concerns about the potential and overall quality of high (30%) and medium (20%) fat sau-
health risks associated with the consumption of food with high sages was related to the aroma compounds, and these con-
content of sodium and fat have led the meat industry to tents of fat were not differentiated by consumers [140].
develop new formulations or modify traditional food products In terms of salt and fat reductions together, Rubio et al.
to contain less sodium and fat [131, 133–135]. These new for- [142] evaluated potential starter lactobacilli strains in low-
mulations confer functionality to fermented meat products that acid fermented sausages (fuets), with reduced salt and fat
could be boosted with the use of indigenous starter cultures. content. In this study, 25% of NaCl was substituted with
Several strategies to reduce salt content could be applied KCl; and the fat pork was reduced a lower proportion than
to small manufacturing industries; the simplest is the direct usual. They achieved a reduction in salt and fat (25% and
reduction of salt content, which is only possible in small pro-
52%, respectively) without detrimental effects on the sensory
portions due to technological contributions of NaCl. Another
quality of the fuets. Mora-Gallego et al. [143] have shown
strategy consists of the partial substitution of NaCl for salts
that even a reduction of 70% of fat in nonacid fermented sau-
such as KCl, CaCl2, or MgCl2. In this sense, KCl is the most
sages resulted in satisfactory overall sensory quality of fuet-
used substitute in fermented meat products and exerts an
type sausages. Mora-Gallego et al. [133] found that the
inhibitory effect on muscle proteases similar to NaCl; but
their main limitation is the metallic flavor [136]. Another reduction of fat proportion (from 20% to 10%) and salt (from
alternative is to modify the salt size; however, the salt size 2.5% to 1.5%) had good consumer acceptability in dry fer-
manipulation in meat products has not been shown yet [131]. mented sausage type fuet, but these simultaneous reductions
Laranjo et al. [135] analysed the effect of salt reduction on led to an increase in aw . The increase of aw was compensated
Portuguese traditional dry-cured sausages. They found that a by an addition of 0.64% KCl, which does not negatively affect
reduction of 50% of salt did not affect the safety of the prod- the consumer acceptability. D. hansenii P2—isolated from
uct but the flavor and the texture. Later, they evaluated the naturally fermented sausages—was used as starter in the pro-
same salt reduction in traditional blood dry-cured sausages, duction of dry fermented sausages manufactured varying salt
which in this case had a positive effect on product acceptance and/or pork back fat content and sensory analysis showed
by the panelists without compromising the microbiological that yeast inoculation improved the aroma and taste quality
stability or fatty acid profile of dry-cured sausages, but bio- when fat or salt reductions were done [144]. The contribu-
genic amine levels increased [137]. Therefore, they propose tion of inoculation to the reformulated dry sausages was
to complement the reduction of salt with the use of starter attributed to the increase in aroma compounds derived from
cultures to minimize the levels of biogenic amines and pro- amino acid degradation and ester activities which increased
mote the development of flavor. the perception of fruity and cured aroma [145]. Nevertheless,
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International Journal of Food Science 9

yeast inoculation did not show a clear effect when salt and fat uals and not able to be readily expressed as it is skill, know-
reduction was carried out together. how, and expertise [151]. Traditional recipes which connected
early European immigrants with their homeland are very com-
7. Additional Support Strategies mon in this target segment, mainly in those countries known as
the “new world” (e.g., Canada, Australia, USA, and Latin Amer-
7.1. Quality Product Registers. In many economic regions, ican communities). Particular raw ingredient compositions are
there exist quality policies aimed at protecting the names of processed according to these recipes that have been passed
specific products to promote their unique characteristics, down from one generation to another. Although certain prob-
linked to their geographical origin as well as traditional lems of product quality variations are recorded, unique flavors
know-how [146]. Fermented meat products, namely, dry from small artisanal firms producing dry sausages are very pop-
sausages, fall into this set of products. The geographical indi- ular among local consumers.
cation (GI) is a sign used on products that have a specific geo- At this point, one of the critical issues in the heart of
graphical origin and possess qualities or a reputation that are leveraging traditional sausage manufacturing with scientific
due to that origin [147]. In the case of foodstuffs and wine, GI developments consists of finding the ways for doing so suc-
comprised Protected Designation of Origin (PDO) and Pro- cessfully. Building on this reasoning, merging tacit and codi-
tected Geographical Indication (PGI). As stated by the fied knowledge seems to be an imperative for scholars if they
WIPO: “In order to function as a GI, a sign must identify a aim to leverage the potential of small artisanal dry sausage
product as originating in a given place. In addition, the qual- local firms. Science, technology, economy, culture, ecosys-
ities, characteristics, or reputation of the product should be tem, and interorganizational synergies are, at least, main
essentially due to the place of origin. Since the qualities aspects for strategies related to territorial networks, produc-
depend on the geographical place of production, there is a tion, and innovation. Promoting multilevel connection
clear link between the product and its original place of pro- among firms, university, and government appears as a master
duction.” From a wider perspective, these quality schemes can hint for leveraging sausage manufacturing clusters which are
play a special role in promoting sustainable rural development, not only sectoral but also geographical. In this sense, there is
improving farm income and opening new export potential. a need for a change in focus to multidimensional and
Geographical indications have to be requested to the cor- specific-context knowledge based on firm-by-firm analysis.
responding national or international authorities; this bureau- Moreover, this new innovation perspective needs a broader
cratic paperwork could be time-consuming; there are legal picture than a microeconomic level; only a micro-meso-
aspects to be fulfilled; and some extra taxes might be applied macro approach may lead to local development as a collective
on the products depending on the legislation. However, the and cooperation-based learning process.
benefits associated with these concepts justify these actions.
Having a GI could broaden the marketing boundaries of arti- 8. Conclusions
sanal dry sausages. Fermented meat products can be added as
local craft elements on touristic routes, embracing the cur- Microbial cultures specifically chosen for any meat fermen-
rent tendency of synergy between tourism, culture, and gas- ted product should help to control undesirable native flora
tronomy. Furthermore, GIs comprise knowledge and skills and give a uniform quality to food in every batch. Technolog-
passed on from generation to generation, helping to protect ical support to incorporate these cultures into the production
local heritage. process might become an indispensable part of innovation
and creativeness for small-scale facilities. A great combina-
7.2. Innovation through Tradition. De Massis et al. [148] con- tion of selected microbial cultures could be designed to offer
ceptualize a new strategic approach, called “innovation improved and/or preserved sensorial attributes among which
through tradition,” which identifies the elements that enter- flavor, overall appearance, texture, and stability of the final
prises possess to profit from leveraging the past, thus com- product are of paramount importance. Even though the
bining tradition and innovation into new products. Within introduction of biotechnology could represent a competitive
the food sector, consumers’ needs tend to be satisfied by advantage for small-scale facilities, typical sensory properties
offering products being able to balance tradition and innova- need to be preserved, particularly when the product is per-
tion [149]. The need for innovation in dry sausages, mainly ceived as rooted in a cultural past that has been dominated
in traditional small-scale manufacture, appears as a big by craftsmanship and it is valued as such.
challenge. Besides safety and health, the meat industry aims at inno-
Small- and medium-sized enterprises (SMEs) need to vation by generating a superior perceived quality while focus-
find ways to maintain and increase their niche markets under ing on traditional flavors. Consumers’ acceptability is the
the pressure of rapid technological changes while the produc- master key for successful product innovation. Herein, several
tion rationale remains as an art. On the one hand, there is a technological processes associated to indigenous microbial
significant development of codified knowledge and on the cultures aimed at improving the quality of artisanal fermen-
other traditional manufacturing practices and skilled sausage ted meat products were presented as potential strategies for
makers with a colorful history. Codified knowledge is explicit small-scale facilities. The authors are aware of the challenge
and consists of facts, theories, and principles that are codified that these implementations would entail considering that
in research journals, taught in universities and recorded in microbial strains should be isolated from each facility. None-
industries [150]. Tacit knowledge is widely held by individ- theless, it might be a reasonable enterprise in the light of the
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10 International Journal of Food Science

benefits that may be gained from these “microscopic facto- [9] M. Ayyash, A. Olaimat, A. al-Nabulsi, and S. Q. Liu, “Bioac-
ries.” Facing the next decade and beyond implies moving for- tive properties of novel probiotic Lactococcus lactis fermented
ward to a more healthy, sustainable, and fair food system. camel sausages: cytotoxicity, angiotensin converting enzyme
Within this context, traditional foods should be used to valo- inhibition, antioxidant capacity, and antidiabetic activity,”
rize niche productions, uphold small-scale producers, and Food Science of Animal Resources, vol. 40, no. 2, pp. 155–
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flavour and safety in fermented sausages: first results of a
cultures and raw matter.
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Conflicts of Interest [11] G. Vignolo, C. Fontana, and S. Fadda, “Semidry and dry fer-
mented sausages,” in Handbook of meat processing, F. Toldr,
The authors declare that they have no conflicts of interest Ed., pp. 379–398, Wiley-Blackwell, Oxford, UK, 2010.
regarding the publication of this paper. [12] L. Aquilanti, C. Garofalo, A. Osimani, and F. Clementi, “Ecol-
ogy of lactic acid bacteria and coagulase negative cocci in fer-
mented dry sausages manufactured in Italy and other
Acknowledgments Mediterranean countries: an overview,” International Food
Research Journal, vol. 23, no. 2, pp. 429–445, 2016.
This work was supported by Consejo Nacional de Investiga-
ciones Científicas y Técnicas de la República Argentina [13] I. Franciosa, V. Alessandria, P. Dolci, K. Rantsiou, and
L. Cocolin, “Sausage fermentation and starter cultures in
(CONICET) (PIP No. 112-201301-00078CO), Agencia Nacio-
the era of molecular biology methods,” International Journal
nal de Investigaciones Científicas y Técnicas de la República of Food Microbiology, vol. 279, pp. 26–32, 2018.
Argentina (ANPCyT) (PICT-2018-0290), and Universidad
[14] N. Palavecino Prpich, O. Garro, M. Romero, M. Judis,
Nacional del Chaco Austral (UNCAus) (PI No. 69-97). M. Cayré, and M. Castro, “Evaluation of an autochthonous
starter culture on the production of a traditional dry fermen-
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