Food Chemistry 201 (2016) 334338

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Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

Short communication

Effect of curing salts and probiotic cultures on the evolution of flavor

compounds in dry-fermented sausages during ripening
Marianthi Sidira a,b, Panagiotis Kandylis a, Maria Kanellaki a, Yiannis Kourkoutas b,
a
Food Biotechnology Group, Section of Analytical Environmental and Applied Chemistry, Department of Chemistry, University of Patras, Patras, GR-26500, Greece
b
Applied Microbiology and Molecular Biotechnology Research Group, Department of Molecular Biology and Genetics, Democritus University of Thrace, Alexandroupolis,
GR-68100, Greece

a r t i c l e i n f o a b s t r a c t

Article history: The effect of the concentration of curing salts, the nature of the probiotic culture (free or immobilized
Received 22 May 2015 Lactobacillus casei ATCC 393 on wheat grains) and the ripening time on the generation of volatile com-
Received in revised form 17 December 2015 pounds in probiotic dry-fermented sausages was investigated. Samples were collected after 1, 28 and
Accepted 19 January 2016
71 days of ripening and subjected to SPME GC/MS analysis. All factors affected significantly the concen-
Available online 21 January 2016
tration of all volatile compounds. Noticeably, the content of esters, organic acids and total volatiles was
significantly increased after 28 and 71 days of ripening in almost all products. In most cases, reduction of
Chemical compounds studied in this article:
curing salts content resulted in significant increase of esters and organic acids during ripening, whereas
Ethanol (PubChem CID: 702)
Acetic acid (PubChem CID: 176)
the opposite effect was observed in carbonyl compounds at days 28 and 71. Principal Component
1-Octen-3-ol (PubChem CID: 18827) Analysis of the semi-quantitative data revealed that primarily the ripening process affected the volatile
2-Phenylethanol (PubChem CID: 6054) composition.
Ethyl lactate (PubChem CID: 7344) 2016 Elsevier Ltd. All rights reserved.
Ethyl hexanoate (PubChem CID: 31265)
Ethyl octanoate (PubChem CID: 7799)
Ethyl decanoate (PubChem CID: 8048)
Hexanal (PubChem CID: 6184)
Octanal (PubChem CID: 454)

Keywords:
HS-SPME GC/MS
Volatiles
Probiotic sausages
Immobilized L. casei ATCC 393
Wheat

1. Introduction stabilization of cells and formulation of new types of foods fortified

with immobilized health-promoting bacteria that are only released
Nowadays there is an upsurge of interest in developing novel upon reaching the human gut (Bosnea et al., 2009; Kourkoutas,
foods containing probiotic microorganisms. Such functional cul- Xolias, Kallis, Bezirtzoglou, & Kanellaki, 2005; Kourkoutas et al.,
tures, apart from conferring a health benefit on the host, may offer 2006; Mattila-Sandholm et al., 2002).
organoleptic and nutritional advantages (Deshpande, Rao, & Patole, Apart from a beneficial to human health product, a unique aro-
2011; Mitropoulou, Nedovic, Goyal, & Kourkoutas, 2013). In this matic profile is an undeniable aim for the food industry. The aroma
context, the meat industry is seeking for suitable starter cultures development in dry-fermented sausages is related to the high
that meet food safety, shelf-life, technological effectiveness and number of changes that occur during fermentation, maturation
economic feasibility criteria (Ammor & Mayo, 2007). and drying. The correlation between the starter culture and the fla-
Immobilization techniques are usually applied in order to main- vor of fermented sausages has been well established (Flores, Dur,
tain cell viability, activity and functionality. Thus, efforts aimed at Marco, & Toldr, 2004) and several studies have been focused on
the improvement of nutritional profile and sensory characteristics
Corresponding author at: Applied Microbiology and Molecular Biotechnology
of fermented sausages (Flores et al., 2004; Marco, Navarro, &
Research Group, Department of Molecular Biology and Genetics, Democritus Flores, 2006; Olivares, Navarro, & Flores, 2009).
University of Thrace, Alexandroupolis, GR-68100, Greece. In dry-fermented sausages, curing salts, such as nitrates and
E-mail address: ikourkou@mbg.duth.gr (Y. Kourkoutas). nitrites are usually added, aiming at growth inhibition of

http://dx.doi.org/10.1016/j.foodchem.2016.01.084
0308-8146/ 2016 Elsevier Ltd. All rights reserved.
 M. Sidira et al. / Food Chemistry 201 (2016) 334338 335

undesirable bacteria in combination to pH reduction which occurs To investigate the effect of curing salts on formation of volatiles,
during fermentation, as well as for color formation. Functional dry-fermented sausages were produced containing 0.02% NaNO2,
starter cultures may be useful in reducing their levels, as the use 0.02% NaNO3 and 2% NaCl (P-samples) or 0.01% NaNO2, 0.01%
of nitrates and nitrites is under discussion because of their contri- NaNO3 and 1% NaCl (RP-samples). Finally, dry-fermented sausages
bution to the formation of health affecting nitrosamines. with no preservatives (NP-samples) were prepared. Ripening was
Among LAB, Lactobacillus casei ATCC 393 strain has been added carried out at room temperature (1923 C with a relative humid-
into food products (Kourkoutas et al., 2005, 2006) to confer probi- ity between 40% and 85%) for 12 days and then the temperature
otic properties (Choi et al., 2006; Saxami et al., 2012; Sidira et al., was decreased to 46 C at a rate of 24 C/day with a relative
2010). humidity between 50% and 75% for up to 71 days.
Immobilized L. casei ATCC 393 cells on wheat grains were suc- All experiments were carried out in triplicate (3 independent
cessfully used in the production of probiotic dry-fermented sau- batches of sausages were prepared). Samples were collected after
sages and the effect of the concentration of immobilized cells 1, 28 and 71 days of ripening and subjected to HS-SPME GC/MS
was studied (Sidira, Karapetsas, Galanis, Kanellaki, & Kourkoutas, analysis to determine the volatile composition.
2014). The presence of the probiotic strain at levels above the
minimum concentration for conferring a probiotic effect
2.4. Head Space (HS) Solid Phase Microextraction (SPME) Gas
(P6 log cfu/g) during ripening and after mild heat treatment
Chromatography/Mass Spectrometry (GC/MS) Analysis
was confirmed by an efficient molecular tool (Sidira, Karapetsas,
et al., 2014), while the immobilized cells had a significant effect
The SPME GC/MS analysis was carried out as described recently
on the volatiles profile during ripening (Sidira, Kandylis,
(Sidira et al., 2015a, 2015b). In brief, grated samples (6 g each)
Kanellaki, & Kourkoutas, 2015a), as well as after heat-treatment
were placed into a 20 ml headspace vial fitted with a Teflon-
(Sidira, Kandylis, Kanellaki, and Kourkoutas, 2015b). In addition,
lined septum sealed with an aluminum crimp seal, through which
the protective effects of the above strain were recently evaluated
the SPME syringe needle (bearing a 2 cm fiber coated with
(Sidira, Galanis, Nikolaou, Kanellaki, & Kourkoutas, 2014) and the
50/30 mm Divinylbenzene/Carboxen on poly-dimethyl-siloxane
results suggested that production of dry-fermented sausages with
bonded to a flexible fused silica core, Supelco, SigmaAldrich,
reduced or negligible amounts of chemical preservatives and salt
Poole, UK) was introduced. The container was then thermostated
is feasible. However, studies concerning the effect of the chemical
at 35 C for 3035 min. The absorbed volatile analytes were then
preservatives and salt, along with probiotic cultures and the ripen-
analyzed by GC/MS (Shimadzu GC-17A, MS QP5050, capillary col-
ing time on volatiles of dry-fermented sausages are scarce in
umn Supelco CO Wax-10 60 m, 0.32 mm i.d., 0.25 lm film thick-
literature.
ness). Helium was used as the carrier gas (linear velocity of
Hence, the objective of the present study was to investigate the
1.8 ml/min). Oven temperature was set at 40 C for 2 min, followed
combined effect of the concentration of the curing salts and the
by a temperature gradient of 10 C/min to 200 C, and then 15 C/
nature of the probiotic culture (free or immobilized L. casei ATCC
min to 250 C. A final extension was applied at 250 C for 5 min.
393 on wheat grains) on the volatile compounds generated in
The injector was operated in splitless mode. Injector and detector
dry-fermented sausages during the maturation process.
temperatures were 280 C and 250 C, respectively. The mass spec-
trometer was operated in the electron impact mode with the elec-
2. Materials and methods tron energy set at 70 eV. The identification was carried out by
comparing the retention times and mass spectra of volatiles to
2.1. Bacterial strain and culture conditions those of authentic compounds generated in the laboratory, by mass
spectra obtained from NIST107, NIST21 and SZTERP libraries, and
L. casei ATCC 393 (DSMZ, Germany) was grown at 37 C for 72 h by determining kovats retention indexes and comparing them
on de Man, Rogosa and Sharpe (MRS) Broth. with those reported in the literature. Kovats retention indexes
were determined by injection of a standard mixture containing
the homologous series of normal alkanes (C8C24) in pure hexane
2.2. Preparation of support and cell immobilization under exactly the same experimental conditions, as described
above. All authentic compounds used were obtained from
Wheat grains were boiled and sterilized at 130 C for 15 min. SigmaAldrich. Methyl octanoate (SigmaAldrich) diluted in pure
Cell immobilization was carried out as described previously hexane was used as an internal standard (IS) at various concentra-
(Bosnea et al., 2009). tions (1.25, 12.5, 125 and 1250 lg/kg of sausage). The volatile com-
pounds were semi-quantified by dividing the peak areas of the
compounds of interest by the peak area of the IS and multiplying
2.3. Production of probiotic dry-fermented sausages
this ratio by the initial concentration of the IS (expressed as lg/
kg). The peak areas were measured from the full scan chro-
Dry-fermented sausages were prepared using traditional tech-
matograph using total ion current (TIC). Each experiment was car-
niques, as described recently (Sidira, Galanis, et al., 2014). In brief,
ried out in triplicate and the mean data are presented (standard
a batch consisting of ground pork meat (2.0 kg), lard (0.5 kg),
deviation for all values was about 10% in most cases).
ground orange peel (25.0 g), ground leek (412.5 g), white pepper
(3.75 g), red pepper (3.75 g), cumin (3.75 g), ground garlic
(1.25 g), oregano (10.0 g), sucrose (15.0 g) and lactose (5.0 g) was 2.5. Experimental design and statistical analysis
inoculated with free (2.5 g wet weight; F-samples) or immobilized
cells of L. casei (250 g wet weight, I-samples) on wheat. After mix- All treatments were carried out in triplicate. The experiments
ing, curing salts were added and the stuffing of natural casings pro- were designed and analyzed statistically by ANOVA. Thus, a
duced fresh sausages. For comparison reasons, sausages with no three-way ANOVA was applied to study the effect of chemical
culture (samples NC) were also produced. Of note, the initial cell preservatives, probiotic cultures and ripening time and the three
counts of L. casei ATCC 393 in probiotic products ranged in levels independent replicates were included as parameters. Duncans
>6 log cfu/g in all cases (when incorporated in either immobilized multiple range test was used to determine significant differences
or free form). among results (coefficients, ANOVA tables and significance
336 M. Sidira et al. / Food Chemistry 201 (2016) 334338

(P < 0.05) were computed using Statistica v.5.0). Principal compo- octanoate, and ethyl decanoate, that have been previously detected
nent analysis (PCA) of data was computed using SPSS (v. 15.0). in dry-fermented sausages (Flores et al., 2004; Marco et al., 2006;
Olivares et al., 2009). Ethyl esters are considered essential for
obtaining the proper fermented sausage aroma by adding a fruity
3. Results and discussion note and masking rancid odors (Flores et al., 2004).
Organic acids consisted an important group of volatile com-
3.1. HS-SPME GC/MS analysis pounds. Medium (C6C12) chain fatty acids mainly derive from
the degradation of lipids and may act as precursors of compounds
For the evaluation of the aromatic profile during ripening, the that have a significant effect on organoleptic properties, but they
dry-fermented sausages were analyzed using the HS-SPME GC/ are not directly responsible for sensory improvements in meat
MS technique. Semi-quantitative results of the volatile compounds products. They basically originate from the lipolytic activity of
are presented in Table 1. In total, 103 compounds were detected. micrococci (Ansorena, Astiasarn, & Bello, 2000). In contrast, short
Esters, organic acids, alcohols and carbonyl compounds were chain fatty acids (C < 6) have greater implications in flavor devel-
the most important compounds identified by the HS-SPME GC/ opment, due to the very strong odors and to their lower threshold
MS technique. Nevertheless, aroma perception in meat products values. Acetic acid detected in all sausages ripened for at least
depends not only on the concentration and odor thresholds of vola- 28 days is produced from fermentation pathways (data not
tile compounds, but also on the interactions with other food com- shown).
ponents and among volatile compounds. The metabolic pathways involved in the biosynthesis of alco-
From a quantitative point of view, all factors (probiotic cultures, hols present in fermented meat products include methyl ketone
chemical preservatives and ripening time) affected significantly reduction, amino acid metabolism and lipid oxidation. Ethanol
(P < 0.05) the concentration of all volatile compounds and a strong identified in all cases was among the most abundant compounds
interaction among them was also observed. Noticeably, the content and is a product of carbohydrate metabolism (data not shown).
of esters, organic acids and total volatiles was significantly Other alcohols that are suggested as important aroma contributors
(P < 0.05) increased after 28 and 71 days of ripening in almost all were 1-octen-3-ol, 2,3-butanediol and 2-phenyl-ethanol. 1-Octen-
products. In most cases, reduction of chemical preservatives 3-ol derives from lipid oxidation and has a characteristic odor of
resulted in significant (P < 0.05) increase of esters and organic acids mushroom and a very low odor threshold (Ansorena, Gimeno,
during ripening, whereas the opposite effect was observed in car- Astiasarn, & Bello, 2001). 2,3-Butanediol is produced by the
bonyl compounds at days 28 and 71. reduction of methyl-ketones from the a-oxidation of fatty acids
Most of the esters identified were ethyl esters, such as ethyl (Marco et al., 2006). 2-Phenylethanol was considered among the
acetate, ethyl propanoate, ethyl butanoate, ethyl 3-methyl- most important odorants in Spanish sausages (Schmidt & Berger,
butanoate, ethyl pentanoate, ethyl hexanoate, ethyl lactate, ethyl 1998).

Table 1
Effect of the concentration of curing salts and the nature of the probiotic culture (free or immobilized Lactobacillus casei ATCC 393 on wheat grains) on the sum of volatile
compounds (lg/kg) isolated from dry-fermented sausages after ripening for 1, 28 and 71 days using the HS-SPME GC/MS technique.

Ripening time Samples Sum of Sum of organic Sum of Sum of carbonyl Sum of miscellaneous Total
(days) esters acids alcohols compounds compounds volatiles
1 I-P 71 3 0.5 60 4 45 3 310 15 425 25
I-RP 50 3 9 0.5 300 15 400 20 2100 110 2800 140
I-NP 135 7 60 3 1500 75 1750 90 11,800 600 15,200 760
F-P 35 2 20 1.0 220 10 280 15 2400 120 3000 150
F-RP Nd 14 1 2000 15 240 10 2400 120 4600 150
F-NP 11 1 90 5 340 20 840 40 6100 300 7300 370
NC-P 36 2 Nd 180 10 360 20 1500 75 2100 100
NC-RP 14 1 8 0.5 450 25 750 40 4700 240 5600 300
NC-NP 4 0.5 20 1 440 20 320 15 3300 160 4000 200
28 I-P 60 3 360 20 820 40 750 40 8800 400 10,800 540
I-RP 150 8 1200 60 640 30 490 25 4600 230 7100 360
I-NP 1800 90 3100 150 1800 90 280 15 10700 550 17,700 880
F-P 160 8 700 35.0 500 25 410 20 5300 300 7100 350
F-RP 220 10 1500 75 380 20 260 15 4600 230 6900 350
F-NP 640 30 2100 100 450 20 55 3 4400 220 7700 390
NC-P 270 10 940 50 1100 55 670 35 11,000 550 14,000 700
NC-RP 420 20 810 40 830 40 270 15 4700 235 7000 350
NC-NP 600 30 880 45 1000 50 240 10 5400 270 8200 400
71 I-P 170 10 490 25 550 30 260 15 3900 200 5400 270
I-RP 370 20 1900 100 760 40 490 25 4700 230 8100 410
I-NP 630 30 1800 90 680 35 110 6 3900 190 7100 350
F-P 140 10 600 30 670 35 320 15 2800 140 4600 230
F-RP 200 10 900 45 430 20 180 10 2900 140 4600 230
F-NP 790 40 3900 200 500 25 235 10 5500 275 11,000 550
NC-P 390 20 630 30 760 40 430 20 5200 260 7400 370
NC-RP 270 10 700 35 450 20 190 10 2700 135 4300 220
NC-NP 500 25 1700 85 930 50 200 10 4400 220 7800 390

I-P: sausages containing immobilized cells of L. casei and preservatives (0.02% NaNO2, 0.02% NaNO3, 2% NaCl); I-RP: sausages containing immobilized cells of L. casei and
reduced amount of preservatives (0.01% NaNO2, 0.01% NaNO3, 1% NaCl); I-NP: sausages containing immobilized cells of L. casei and no preservatives; F-P: sausages containing
free cells of L. casei and preservatives (0.02% NaNO2, 0.02% NaNO3, 2% NaCl); F-RP: sausages containing free cells of L. casei and reduced amount of preservatives (0.01% NaNO2,
0.01% NaNO3, 1% NaCl); F-NP: sausages containing free cells of L. casei and no preservatives; NC-P: sausages containing no starter culture and preservatives (0.02% NaNO2,
0.02% NaNO3, 2% NaCl); NC-RP: sausages containing no starter culture and reduced amount of preservatives (0.01% NaNO2, 0.01% NaNO3, 1% NaCl); NC-NP: sausages
containing no starter culture and no preservatives, ND: not detected.
 M. Sidira et al. / Food Chemistry 201 (2016) 334338 337

Fig. 1. PCA plot of volatiles generated during ripening of probiotic dry-fermented sausages. I-P: sausages containing immobilized cells of L. casei and preservatives (0.02%
NaNO2, 0.02% NaNO3, 2% NaCl); I-RP: sausages containing immobilized cells of L. casei and reduced amount of preservatives (0.01% NaNO2, 0.01% NaNO3, 1% NaCl); I-NP:
sausages containing immobilized cells of L. casei and no preservatives; F-P: sausages containing free cells of L. casei and preservatives (0.02% NaNO2, 0.02% NaNO3, 2% NaCl);
F-RP: sausages containing free cells of L. casei and reduced amount of preservatives (0.01% NaNO2, 0.01% NaNO3, 1% NaCl); F-NP: sausages containing free cells of L. casei and
no preservatives; NC-P: sausages containing no starter culture and preservatives (0.02% NaNO2, 0.02% NaNO3, 2% NaCl); NC-RP: sausages containing no starter culture and
reduced amount of preservatives (0.01% NaNO2, 0.01% NaNO3, 1% NaCl); NC-NP: sausages containing no starter culture and no preservatives. Ripening days are indicated after
sample codes.

Aldehydes and ketones were the main carbonyl compounds the curing salts also had a significant effect. However, it is yet
detected (data not shown). Most of the carbonyl compounds unknown and difficult to interpret the relationships between the
identified, like pentanal, hexanal, heptanal, 2-hexenal, octanal, 1- microbial associations which are involved in the biochemical
octen-3-one, 2-heptenal, nonanal, 2-octenal, 2-nonenal, butyrolac- changes that occur during ripening of fermented sausages, the cur-
tone, 2-decenal, and 2,4-nonadienal may come from lipid oxidation ing salts and the chemical compounds, due to the high complexity
and are usually present in dry-fermented sausages (Ansorena et al., of the food ecosystem.
2001; Marco et al., 2006). High molecular aldehydes are not con-
sidered major contributors to the aroma, but their importance to 4. Conclusions
flavor development is only due to the fact that they can act as pre-
cursors of lower molecular alkanals and alkenals (Ansorena et al., In conclusion, the concentration of curing salts, the nature of
2001). the probiotic culture (free or immobilized L. casei ATCC 393 on
A number of miscellaneous compounds were also detected, wheat grains) and the ripening time had a significant effect on
including terpenes, sulfur compounds and hydrocarbons (data the concentration of all volatile compounds. Of note, PCA showed
not shown). Terpenes may derive by spices, although some of them that primary the ripening process affected the volatile profile. Gen-
have been found in meat as a consequence of their presence in ani- erally, reduction of curing salts led to increased content of esters
mal feedstuffs, while some sulfur compounds identified may come and organic acids. However, more research is required to better
from garlic (Ansorena et al., 2000, 2001). Hydrocarbons are not understand the microbial interactions which are responsible for
considered as important contributors to the odor profile. the biochemical changes that occur during the ripening process
of dry-fermented sausages and the effect of the curing salts on
3.2. Chemometrics volatiles.

The application of the PCA algorithm to data showed four dis- Acknowledgments
tinctive groups (Fig. 1). The first group was composed by samples
ripened for 28 and 71 days, except from samples I-NP-28 and This research has been co-financed by the European Union
NC-P-28 which consisted the second group. The third group con- (European Social Fund ESF) and Greek national funds through
tained only sausages ripened for 1 day. A fourth group containing the Operational Program Education and Lifelong Learning of
only I-NP-1 sample was also evident. The results of PCA indicated the National Strategic Reference Framework (NSRF) Research
that primarily the ripening time affected the volatile composition Funding Program: Heracleitus II. Investing in knowledge society
of dry-fermented sausages, although the probiotic culture and through the European Social Fund.
338 M. Sidira et al. / Food Chemistry 201 (2016) 334338

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