Meat Science 154 (2019) 29–36

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Incorporation of probiotic strain in raw minced beef meat: Study of textural T

modification, lipid and protein oxidation and color parameters during
refrigerated storage
Imen Trabelsia,1, Sirine Ben Slimaa,1, Naourez Ktarib, Mehdi Trikic, Rania Abdehedid,
⁎
Wafa Abazaa, Hafedh Moussac, Asehraou Abdeslame, Riadh Ben Salaha,
a
Laboratory of Microorganisms and Biomolecules (LMB), Centre of Biotechnology of Sfax, Road of Sidi Mansour Km 6, P.O. Box 1177, Sfax 3018, Tunisia
b
Laboratory of Enzyme Engineering and Microbiology, University of Sfax, National School of Engineering of Sfax (ENIS), B.P. 1173, 3038 Sfax, Tunisia
c
Chahia Company, Road of Gabes km 1 ZI Sidi Salem, 3002 Sfax, Tunisia
d
Laboratory of Molecular and Cellular Screening Processes, Center of Biotechnology of Sfax, P. O. Box 1177, 3018 Sfax, Tunisia
e
Laboratory of Biochemistry and Biotechnology, Faculty of Sciences, University Mohammed Premier, Oujda, Morocco

A R T I C LE I N FO A B S T R A C T

Keywords: The aim of this work was to evaluate the effect of different concentrations of probiotic strain Lactobacillus
L. plantarum TN8 plantarum TN8 on the quality and safety of raw minced beef after 10 days of refrigerated storage. The obtained
Raw minced beef meat results showed that the incorporation of the probiotic strain can inhibit the proliferation of spoilage micro-
Texture profile organisms, such Listeria monocytogenes and Salmonella spp., delay the lipid oxidation, improve texture para-
Color parameters
meters, and extend the shelf life of these products during storage. We also examined the correlations between
Biopreservative
protein and lipid oxidation, texture profile and color parameters of raw minced beef meat inoculated with L.
plantarum TN8. The incorporation of strain at 108 CFU/g resulted in better quality inclusive color, lipid oxidative
stability, and texture parameters notably cohesiveness, adhesiveness, hardness and chewiness. Overall, the
findings demonstrated that TN8 can be used as a biopreservative agent for extending the safety and quality of
refrigerated raw minced beef meat.

1. Introduction antioxidative activities (Smaoui et al., 2017), which could have an ef-
fect on chemical processes including lipid and protein oxidation and
During storage, biochemical reactions and microbial growth could thus could enhance the quality of meat products. LAB including Lac-
be deteriorate meat and meat products due to their biological char- tobacillus, Pediococcus, Bifidibacterium, Bacillus, and Enterococcus
acteristics and chemical composition such as of saturated and un- (Bomdespacho, Cavallini, Zavarizi, Pinto, & Rossi, 2014; Jafari et al.,
saturated lipids, proteins, carbohydrates, vitamins, and pigments 2017; Sparo, Confalonieri, Urbizu, Ceci, & Bruni, 2013) have success-
(Pateiro et al., 2018). These alterations affect the quality of the final fully been applied in meat products.
products and notably their acceptability to the consumer (Iulietto, Probiotic cultures may be supplemented to the sausage as liquid
Sechi, Borgogni, & Cenci-Goga, 2015). Biopreservation is a developed inoculum, in high concentrations, or lyophilized. As well as, probiotic
alternative technique used to maintain safety, microbiological quality strains isolated from human intestines could be incorporated in meat
and to extend food shelf-life of meat and meat products. In fact, the products. Indeed, they should be competent with the bacteria presented
application of a protective microbiota, such as lactic acid bacteria (LAB) in meat. They are also supposed to survive the process of fermentation
with their metabolic products such as bacteriocin, organic acids, hy- and that of refrigerated storage (Kołozyn-Krajewskaa & Dolatowski,
drogen peroxide, and enzymes has been investigated in several re- 2012). LAB are commonly used as probiotic strains (Campana, van
searches (da Costa, Voloski, Mondadori, Duval, & Fiorentini, 2019). Hemert, & Baffone, 2017). Probiotics are defined by a joint FAO/WHO
Various LAB strains have been shown also to possess a power working group as “live microorganisms which, when administered in

⁎
Corresponding author at: Laboratoire de Microorganismes et de Biomolécules (LMB), Centre de Biotechnologie de Sfax, Route de Sidi Mansour Km 6, BP 1177,
3018 Sfax, Tunisia.
E-mail address: [email protected] (R. Ben Salah).
1
The two authors have contributed equally to this work.

https://doi.org/10.1016/j.meatsci.2019.04.005
Received 30 October 2018; Received in revised form 23 February 2019; Accepted 3 April 2019
Available online 04 April 2019
0309-1740/ © 2019 Published by Elsevier Ltd.
I. Trabelsi, et al. Meat Science 154 (2019) 29–36

adequate amounts, confer good health benefit on the host” by im- were triplicate by producing different batches on separate days. All
proving its intestinal microbial balance (FAO/WHO, 2002). The ma- quality parameters were measured in triplicate. Thus the total samples
jority of probiotic species are frequently isolated from the intestinal analyzed were 144 (48 × 3).
microflora of the intended users (e.g., human, pig or chicken) and se-
lected on some probiotic criteria such as resistance to stomach acids, 2.3. Chemical composition of beef meat
lysozyme and bile salts, ability to colonize the intestine using me-
chanisms of adhesion or binding to intestinal cells (Ben Salah, Trabelsi, AOAC, 2005 was used to determine Moisture and ash contents of
Hamden, Chouayekh, & bejar, 2013; Cho, Zhao, & Kim, 2011). In ad- beef meat and Kjeldahl technical was used to determine protein con-
dition to their metabolic secretion and physiological characteristics, tents according to standard method 984.13, estimated by multiplying
they receive market interest as functional meat and meat products. total nitrogen content by a factor of 6.25 (AOAC, 2000) and analyzed
The development of functional food promotes health and well- on the 10th day of storage.
being, beyond their nutritional benefits (Grasso, Brunton, Lyng, Lalor,
& Monahan, 2014). “Functional food”, contains ingredients emanating 2.4. pH and texture profile analysis (TPA) of beef meat
from natural sources that should regulate physiological functions of the
human body delaying retarding aging and improving the immune pH was determined with a pH meter (744, MettlereToledo GmbH,
system against diseases (Zhang, Xiao, Samaraweera, Lee, & Ahn, 2010). Schwerzenbach, Switzerland) by direct insertion into the samples. Prior
Therefore, probiotic strains have attracted an increasing interest as to use, the pH meter was calibrated using three Metrohm buffer solu-
their consumptions offers health benefits to consumers. tions whose pHs were 4, 7, and 9, at room temperature.
Taking into account all the above mentioned benefits, the aim of Using a texture analyzer (TA-XT2i, Stable Micro Systems Ltd.,
this work was to incorporate a probiotic strain, L. plantarum TN8, in raw Surrey England), the TPA of raw meat beef was evaluated as described
minced beef meat. Physico-chemical, color, textural and micro- by Bourne (1978). The texture analysis conditions were used as de-
biological properties were investigated during storage at 4 °C. The re- scribed by Ben Slima et al. (2017), texture parameters (hardness,
lation between lipid and protein oxidation and sample, color and tex- springiness, adhesiveness, chewiness, and cohesiveness) were quanti-
tural parameters after 10 days of storage was also reported. fied during 10 days of storage at 4 °C. They were measured after
blooming for 30 min (4 °C) at day 0, and then measured immediately
2. Materials and methods after opening packages at 4, 7, and 10 days.

2.1. Bacterial strains and culture conditions 2.5. Determination of color of beef meat

In our laboratory, L. plantarum TN8 strain was isolated from poultry A Color Flex spectrocolorimeter (Hunter Associates Laboratory Inc.,
gastro intestinal tract. This strain exhibited antimicrobial activity Reston, VA, USA, Illuminant D65, 2.54 cm diameter aperture, 10°
against 4 pathogenic bacteria. It showed good resistance to pH 3 and standard observer) was used to determine color parameters of raw
5% bovine bile, sensitivity to several antibiotics, high adhesion and meat. L* refers to lightness measure, b* to the chromatic scale from
anti-inflammatory profiles (Ben Salah et al., 2012). It was cultivated in blue to yellow and a* to the chromatic scale from green to red (Chen,
de Man Rogosa and Sharpe medium (MRS) (Difco, Detroit, MI, USA) for Zhu, Zhang, Niu, & Du, 2010). The black glass and white tile were used
24 h at 30 °C as previously described by Ben Salah et al. (2012). The to standardize the equipment. Determination of color was carried out in
inoculums were prepared as follows: cells were harvested by cen- triplicate.
trifugation at 3000 ×g for 20 min and washed twice with phosphate
buffer saline at pH 7. Cell counts were determined by the standard plate 2.6. Lipid oxidation
method after 48 h under anaerobic conditions on MRS agar and at
30 °C. The relation between CFU/g and OD was determined by standard The extent of lipid oxidation in different samples was assessed
plate method on MRS agar (48 h, 30 °C) (Ben Slima et al., 2017). The through the determination of thiobarbituric acid reactive substances
cell suspensions were then directly used as free cells in the product. (TBARS) such as malondialdehyde (MDA). TBARS was estimated ac-
cording to the method of Ben Slima et al. (2017).
2.2. Preparation and conditioning of meat samples The MDA was determined using the following equation:
mg MDA eq/kg = (A corrected × VTCA × 2 × MMDA .10−2)/(1.56 × m)
Fresh meat beef was obtained from a local meat processing company
(CHAHIA, Sfax, Tunisia). The preparation of meat samples with and where:
without probiotic strain were made as described below. Four equal
A corrected = A532 nm − [((A508 nm − A600 nm) × (600–532))
portions of 300 g of meat were placed separately in sterile plastic bags,
then probiotic strains were added: T1 (Fresh meat beef incorporated /(600/508)] − A600 nm
with L. plantarum at 7 log CFU/g), T2 (Fresh meat beef incorporated
with L. plantarum at 8 log CFU/g), and T3 (Fresh meat beef in- VTCA: Volume of TCA;
corporated with L. plantarum at 9 log CFU/g). A control sample without M: Molecular weight of MDA.
probiotic strain supplementation was used (C). For each experiment, all m: Weight of samples.
runs were applied to a batch of raw beef meat. Each formulation pro-
duced one homogeneous mixture which was vacuum stuffed into plastic 2.7. Metmyoglobin (MetMb) analysis
casings to produce three ‘replicates’. On the tenth day, samples were
analyzed for physicochemical analyses (pH, chemical composition, The contents of MetMb in ground beef meat was estimated ac-
thiobarbituric acid reactive substances (TBARS) metmyoglobin cording to the method of Smaoui et al. (2017). Briefly, 5 g samples were
(MetMb), color, and texture profile). Microbiological analysis was also mixed in 25 ml ice-cold 40 mM phosphate buffer (pH 6.8) for 10 s and
performed. The number of total samples analyzed was 96: (48 × 2). In was kept then for 1 h at 4 °C. After centrifugation at 4500 g for 30 min,
fact, for each analysis (physico-chemical and microbiological analyses the supernatant was filtered through Whatman filter paper and the
48 (4 × 3 × 4) trials were designed as follows: Four treatments absorbance was measured at 572, 565, 545 and 525 nm. The percen-
(Control (C) and three treated meat were realized in triplicate samples tages of MetMb were calculated as follows based on these absorbance
and for each period (0, 4, 7 and 10 days of storage). The treatments values according to Smaoui et al. (2017).

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I. Trabelsi, et al. Meat Science 154 (2019) 29–36

MetMb% = [−2.51(A572/A525) + 0.777(A565/A525) + 0.8(A545/A525) in the use of probiotic strain inoculated in ground beef meat. During
storage, pH values in beef meat treated with 109 CFU/g of L. plantarum
+ 1.098] × 100
were significantly lower than others treated samples (107 and 108 CFU/
g) (P < .05). The results showed similarity with previous studies by
2.8. Microbiological analysis Ben Slima et al. (2017) who indicated that the acidification of probiotic
beef sausage samples is due to the production of lactic acid by the lactic
Microbial analysis was determined during 10 days of storage at 4 °C acid bacteria. pH decline contributes to pathogenic bacteria inhibition
as described below: Lactic acid bacteria (LAB) were cultured in MRS and firmness, flavor and sliceability improvements (Ben Slima et al.,
medium, incubated at 30 °C for 48 h. Enterobacteriaceae counts were 2017).
determined on Violet Red Bile Glucose Agar (VRBGA, Merck, Germany)
at 37 °C for 48 h. To check the presence of Salmonella spp. and Listeria 3.1.3. Lipid oxidation TBARS
spp., we used ISO 6579:, 2002 and ISO11290:2004 methods, respec- Chemical deterioration, especially secondary lipid oxidation, is a
tively. Microbial counts were carried out in triplicate. main factor of limiting the shelf-life of products which causes off-ar-
omas in meat (Smaoui et al., 2016). TBARS values represent the content
2.9. Statistical analysis of lipid peroxidation and results are given in Table 2. They were af-
fected (P < .05) by storage period. Lipid oxidation values increased
SPSS program (V17.0) was applied for each parameter (treatments significantly (P < .05) from 0.46 mg MDA/kg on the first day of sto-
and storage period) using a one-way analysis of variance (ANOVA). rage to 1.50–2.26 mg MDA/kg at the end of storage at 4 °C. Over the
Means and standard errors (SE) were calculated. P < .05 is the prob- refrigerated storage period, TBARS values were lower in treated sam-
ability level used in testing the statistical significance of all experi- ples than the control (C) (P < .0.5). Campo et al. (2006) used MDA
mental data. Tukey's post hoc test was used to determine significance of concentrations around 2 mg/kg as threshold index for oxidized beef
mean values for multiple comparisons at (P < .05). Treatments (con- acceptability. Endogenous lipases and bacterial lipolytic enzymes con-
trol or reformulated samples), storage time (days), and their interac- tributed to the release of free fatty acids (Ben Slima et al., 2018; Chen,
tions were included as fixed effects while batch was included as a Kong, Han, Xia, & Xu, 2017). The free fatty acid synthesis was the main
random effect. All analyses and experiments, including the manu- precursor of volatile compounds which causes lipid oxidation (Gianelli,
facturing processes, were realized in triplicate to guarantee the accu- Salazar, Mojica, & Friz, 2012). In fact, the antioxidant properties could
racy of results and the repeatability of the processes. Multiple stepwise be associated with a higher conjugated linoleic acid (CLA) content.
regression analyses were performed using a Durbin–Watson statistic (Chae, Keeton, & Smith, 2004; Hur et al., 2004; Özer, Kılıç, & Kılıç,
tests to evaluate independent association between lipid and protein 2016). On the other hand, the cis-12, trans-10 CLA isomer exhibited
oxidation and sample, color and textural parameters after 10 days of antioxidant activities over a wide range of concentrations, whereas at
storage. high concentrations, the trans-11, cis-9 CLA isomer was actually con-
sidered as pro-oxidant (Leung & Liu, 2000). In this study, we indicate
3. Results and discussion that probiotic strain addition leads to the decrease of lipid oxidation.
We can explain this finding by the antimicrobial effect of bacteriocin
3.1. Physico-chemical analysis of raw minced beef meat (Smaoui et al., 2014; Smaoui et al., 2017). Popova (2017) reported that
the reduction of TBARS value in poultry meat is due to dietary probiotic
3.1.1. Proximate analysis of raw minced beef meat supplementation. Other results confirm the fact that probiotics present
Moisture contents in the beef meat inoculated with L. plantarum TN8 antioxidant activity in both in vivo and in vitro experiments
at different concentrations (72.85–73.49%) were comparable to control (Abdurrahman, Pramono, & Suthama, 2016; Pieniz, Andreazza,
sample (73.23%) (Table 1). Also, no significant effects on ash and Anghinoni, Camargo, & Brandelli, 2014). Also, Özer et al. (2016) ob-
protein contents were observed between control and treated samples served that lower TBARS values were observed on incorporated sausage
(P > .05). The same results were also reported by previous studies with L. plantarum compared to the control. So, this difference was in-
(Ben Slima et al., 2017). Probiotic strain addition maintains not only evitable during fermentation rest and storage period.
the chemical composition of ground beef meat, but also has a positive
impact for consumers' health when consumed in adequate amounts 3.1.4. Metmyoglobin analysis
(Kołozyn-Krajewskaa & Dolatowski, 2012). Fresh meat color is an interesting quality attribute and characteristic
in the acceptance of the consumers. In fact, brown MetMb formation is
3.1.2. Measurement of pH often attributed to the oxidation of three ferrous oxidation forms in a
The changes in pH levels during refrigerated storage for 10 days are ferric state and is related to meat discoloration (Suman & Joseph,
shown in Table 2. The pH values of ground beef meat inoculated with 2013). This undesirable color of fresh meat is an early warning of
probiotic strain, especially the treatment (T3) showed a decline com- spoilage.
pared to control sample (P < .05). The decrease in pH values resulted Table 1 shows the MetMb formation during storage of ground fresh
beef meat. MetMb formations are increased significantly during the
Table 1 storage period for control and treated samples (P < .05).The percen-
Proximate analysis (%) of ground beef meat at 10th day of refrigerated storage. tage of MetMb was rapidly increased on the 7th day and reached the
limit accepted value 46.03% (Reddy, Mandal, Sen, & Reddy, 2015) in
Samples Moisture Ash Protein content
control (C). However, the MetMb% values in treated samples (38.18,
Control 26.77 ± 0.10a 1.05 ± 0.04a 20.30 ± 0.39 a 32.22 and 29.98 for T1, T2, T3, respectively) were lower than the
T1 27.15 ± 0.49a 1.03 ± 0.04a 20.00 ± 0.57 a
control without probiotic strain added (P < .05). At the end of storage,
T2 26.60 ± 0.08a 1.00 ± 0.06a 20.05 ± 0.11 a
the MetMb% of the treated samples reached the limit accepted
T3 26.99 ± 0.48a 1.06 ± 0.77a 20.40 ± 0.17 a
(Table 2). Our results are in corroboration with Talon, Walter, and
Control:fresh beef meat without probiotic strain, T1, T2, T3: groups of beef Montel (2000) who reported that Lactobacillus and Staphylococcus can
sausages formulated with L. plantarum at 7 log CFU/g, at 8 log CFU/g and at 9 reduce MetMb (MbFe3+) to native myoglobin Mb (Fe2+) and inhibit
log CFU/g, respectively. the unsaturated fatty acids oxidation. Probiotic strains have an influ-
Values are ± standard error of three replicates. a: letter is not significantly ence on the oxidation-reduction potential of meat (Kołozyn-Krajewskaa
different (P > .05) between formulations. & Dolatowski, 2012).

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Table 2
Effect of probiotic strain incorporation on pH, MetMb (%), TBARS (mg MDA/kg meat) of beef meat during storage at 4 °C.
Days of storage at 4 °C 0 4 7 10

pH
Control 5.90 ± 0.01cA 6.01 ± 0.02cB 5.93 ± 0.01cA 6.01 ± 0.02dB
T1 5.77 ± 0.02bA 5.89 ± 0.01bC 5.87 ± 0.01bBC 5.84 ± 0.01cB
T2 5.76 ± 0.01bA 5.89 ± 0.02bC 5.84 ± 0.02bB 5.78 ± 0.02bA
T3 5.61 ± 0.01aB 5.63 ± 0.00aB 5.61 ± 0.02aB 5.41 ± 0.02aA

TBARS
Control 0.46 ± 0.006aA 0.68 ± 0.02bB 1.99 ± 0.09cC 2.26 ± 0.16cD
T1 0.47 ± 0.007aA 0.61 ± 0.01aB 1.35 ± 0.10bC 1.83 ± 0.06bD
T2 0.47 ± 0.005aA 0.60 ± 0.02aB 1.32 ± 0.09abC 1.59 ± 0.09aD
T3 0.47 ± 0.019aA 0.58 ± 0.03aA 1.17 ± 0.09aB 1.50 ± 0.12aC

MetMb
Control 13.30 ± 0.46aA 23.56 ± 0.71dB 46.03 ± 0.67dC 63.86 ± 0.89bD
T1 13.28 ± 0.62aA 21.90 ± 0.55cB 38.18 ± 0.72cC 46.58 ± 3.91aD
T2 13.38 ± 0.54aA 20.24 ± 0.34bB 32.22 ± 0.90bC 44.74 ± 0.99aD
T3 13.26 ± 0.79aA 19.13 ± 0.40aB 29.98 ± 0.75aC 43.53 ± 0.49aD

Control:fresh beef meat without probiotic strain, T1, T2, T3: groups of beef sausages formulated with L. plantarum at 7 log CFU/g, at 8 log CFU/g and at 9 log CFU/g,
respectively.
Values are ± standard error of three replicates. a, b, c: Different letters are significantly different (P < .05) between formulations.
A,B,C: letters are significantly different (P < .05) between storage days within the same formulation.

3.2. TPA analysis displayed an increase in this parameter during the storage period from
1 to 10 days (P < .05). Ganhão, Morcuende, and Estévez (2010) re-
Texture is a predominant element of the acceptability and quality of ported that hardness increases during storage of cooked meat products.
meat products. Results of the TPA parameters of ground beef according It is obvious that the increase of hardness in meat was caused by the
to L. plantarum TN8 supplementation during refrigerated storage are development of protein oxidation products such as carbonyl formation,
presented in Table 3. The highest hardness value was observed in T2 MetMb accumulation, and the reduction of sulphydryl groups through
and T3 samples on the 4th day, whereas the lowest hardness value was the protein functionality loss (Sirinivasan, Xiong, & Decker, 1996). The
observed in control (P < .05). After 10 days of storage at 4 °C, the results also show that the beef meat treated with probiotic strain ex-
hardness value of the control was 2.47 N against 2.22, 2.23 and 2.11 N hibits a significant reduction (P < .05) of springiness and chewiness
for T1, T2 and T3, respectively. Moreover, all reformulated samples than control sample (Table 3). Ben Slima et al. (2017) also reported that

Table 3
Effect of probiotic strain on hardness (N), cohesiveness, adhesiveness (N) springiness (mm) and chewiness (Nmm) of beef meat during storage at 4 °C.
Days of storage at 4 °C 0 4 7 10

Adhesiveness
Control 0.79 ± 0.01aA 0.80 ± 0.05aA 0.89 ± 0.07aA 1.25 ± 0.09aB
T1 0.79 ± 0.01aA 0.96 ± 0.09abB 0.90 ± 0.09aAB 1.24 ± 0.09aC
T2 0.80 ± 0.01aA 1.10 ± 0.09bcB 0.85 ± 0.12aA 1.18 ± 0.12aB
T3 0.79 ± 0.03aA 1.21 ± 0.12cB 0.90 ± 0.07aA 1.14 ± 0.15aB

Hardness
Control 1.53 ± 0.036aAB 1.46 ± 0.02aA 1.69 ± 0.21aBC 2.47 ± 0.12bC
T1 1.57 ± 0.058aA 1.89 ± 0.03bB 1.75 ± 0.14aB 2.22 ± 0.07aC
T2 1.57 ± 0.022aA 2.27 ± 0.01cC 1.84 ± 0.18abB 2.23 ± 0.13aC
T3 1.51 ± 0.040aA 2.28 ± 0.12cB 2.12 ± 0.18bB 2.11 ± 0.14aB

Cohesiveness
Control 0.53 ± 0.02aA 0.56 ± 0.006bA 0.49 ± 0.05aA 0. 51 ± 0.09aA
T1 0.52 ± 0.04aA 0.52 ± 0.017aA 0.51 ± 0.02aA 0.51 ± 0.10aA
T2 0.53 ± 0.03aAB 0.57 ± 0.011bC 0.54 ± 0.04aAB 0.48 ± 0.05aA
T3 0.50 ± 0.02aA 0.53 ± 0.006aA 0.52 ± 0.03aA 0.49 ± 0.06aA

Springiness
Control 2.78 ± 0.06aA 3.82 ± 0.11cC 3.27 ± 0.19cB 3.44 ± 0.15cB
T1 2.75 ± 0.08aA 3.11 ± 0.09bB 3.09 ± 0.16cB 3.62 ± 0.14bcB
T2 2.78 ± 0.06aAB 2.78 ± 0.16aAB 2.55 ± 0.30bA 3.00 ± 0.17abB
T3 2.76 ± 0.08aB 2.64 ± 0.15aB 2.12 ± 0.21aA 2.82 ± 0.59aA

Chewiness
Control 2.56 ± 0.04aA 3.13 ± 0.09cB 3.14 ± 0.13bB 4.11 ± 0.08cB
T1 2.60 ± 0.04aA 2.94 ± 0.09bB 2.53 ± 0.31aA 3.86 ± 0.11cC
T2 2.50 ± 0.19aAB 2.71 ± 0.03aB 2.35 ± 0.21aA 3.60 ± 0.19bC
T3 2.49 ± 0.15aAB 2.68 ± 0.42aB 2.27 ± 0.11aA 3.15 ± 0.17aC

Control: fresh beef meat without probiotic strain, T1, T2, T3: groups of beef sausages formulated with L. plantarum at 7 log CFU/g, at 8 log CFU/g and at 9 log CFU/g,
respectively.
Cohesiveness (N/A), Hardness (N), Springiness (mm), Adhesiveness (N) and Chewiness (Nmm).
Values are ± standard error of three replicates. a, b, c: Different letters are significantly different (P < .05) between formulations. A,B,C: letters are significantly
different (P < .05) between storage days within the same formulation.

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Table 4
Effect of probiotic strain on instrumental color parameters (CIE a*, b*, L*) of beef meat during storage at 4 °C.
Days of storage at 4 °C 0 4 7 10

Color parameters
a*value
Control 5.61 ± 0.14aB 5.04 ± 0.87aB 4.13 ± 0.34aA 9 0.66 ± 0.43aC
T1 5.67 ± 0.13aB 6.06 ± 0.69abC 4.59 ± 0.15abA 11.16 ± 0.49bD
T2 5.66 ± 0.16aAB 6.63 ± 1.11bB 4.83 ± 0.15bA 11.30 ± 0.46bC
T3 5.74 ± 0.17aB 6.75 ± 0.39bC 4.92 ± 0.41bA 11.97 ± 0.46bB
b* value
Control 8.86 ± 0.21aA 9.32 ± 0.22aA 9.24 ± 0.46aA 8.46 ± 0.17bA
T1 8.70 ± 0.41aA 8.74 ± 0.71aA 9.15 ± 0.09aA 7.64 ± 0.76aA
T2 8.80 ± 0.30aA 8.48 ± 0.18aA 9.12 ± 0.61aA 8.89 ± 0.30bA
T3 8.76 ± 0.44aA 8.43 ± 0.69aA 7.94 ± 1.34aA 8.68 ± 0.16bA
L* value
Control 49.58 ± 0.57aB 49.15 ± 0.18bAB 48.24 ± 0.79aA 49.42 ± 0.77aB
T1 49.50 ± 0.75aA 48.24 ± 1.42abA 49.14 ± 0.58abA 47.62 ± 1.43aA
T2 49.59 ± 0.80aA 49.02 ± 1.52bA 50.28 ± 0.83bA 48.75 ± 0.87aA
T3 49.33 ± 0.86aB 46.34 ± 0.86aA 51.63 ± 0.76cC 47.98 ± 1.22aAB

Control: fresh beef meat without probiotic strain, T1, T2, T3: groups of beef sausages formulated with L. plantarum at 7 log CFU/g, at 8 log CFU/g and at 9 log CFU/g,
respectively. Values are ± standard error of three replicates. a, b: Different letters are significantly different (P < .05) between formulations. A,B,C: letters are
significantly different (P < .05) between storage days within the same formulation.

probiotic strain decreases chewiness. The decrease of springiness was

demonstrated by Riebroy, Benjakul, and Visessanguan (2008). On the
other hand, the treated samples were very close to the control sample in
terms of cohesiveness and adhesiveness, values ranged between 0.48
and 0.57 and 0.79–1.25, respectively. In fact, Nowak, Von Mueffling,
Grotheer, Klein, and Watkinson (2007) reported that cohesiveness and
adhesiveness presented important roles for sliced meat. In fact, the
increase of these parameters presents tough and unappealingly sticky
products effects.

3.3. Color parameters

Meat color is important to consumers. At the beginning of the beef

meat processing, no differences in color parameters were found be-
tween meat treated by L. palntarum TN8 and the control sample. Fig. 1. OD600 and log CFU/ml linear relation of L. plantarum TN8 in MRS
medium.
According to the data of fresh ground meat products presented in
Table 4, the products treated with L. plantarum TN8 showed a sig-
nificant (P < .05) increase of a* value than the control sample after concentration of living cells in MRS from OD600 values. From this
4 days of storage. This result is in total agreement with those reported equation, the 1OD value was estimated at about 109 CFU/ml (Fig. 1).
by Ben Slima et al. (2018), who studied the color of beef sausages Enumeration of viable cells during storage period was performed not
treated with probiotic strains during storage. Similar findings were only to assess the viability of the selected probiotic strain, but also to
reported by Hacik et al. (2015). For L* parameter, it decreased on the monitor the bacterial contamination.
4th day of storage in meat iinoculated with probiotic strain. Aristides,
Paiao, Murate, Oba, and Shimokomaki (2012) and Liu et al. (2012) 3.4.1. The lactic acid bacteria counts (LAB)
reported that the probiotic supplementation reduced lightness in the Probiotic strains named, Lactobacillus, are considered as “GRAS”
meat of chickens. However, L* increased on 7th day of refrigerated bacteria that are safe to consume, and are widely incorporated in food
storage, rising, from 48.249 to 51. 63 in ground meat. This change product (Bredholt, Nesbakken, & Holck, 2001). These bacteria have
reflects the effective role in preserving of meat products instead of also the efficiency to be used in food biopreservation, due to their
being decreased through deterioration and oxidation (Triki et al., ability to produce antimicrobial substances such as bacteriocins and
2017). In the case of b* value, ground beef meat was not affected by the lactic acid (De Martinis & Freitas, 2003).
incorporation of L. plantarum TN8 during the refrigerated storage The LAB counts in beef meat were shown in Fig. 2 A. As demon-
period. Our results are in agreement with the findings of Pereira, strated, at the beginning of storage, treatments incorporated with
Soares, Monteiro, Gomes, and Pintado (2018) who reported that the probiotic strain presented significantly higher LAB counts in the beef
presence of Lactobacillus casei or Bifidobacterium animalis did not affect meat than in the control sample without probiotic strain added
(P > .05) the b* color parameter of the sliced ham. Jiang, Jiang, Zhou, (P < .05). The probiotic bacteria counts increased significantly
Lin, and Zheng (2014) reported that lower b* values designate less pale (P < .05) to 12.9, 13.5, and 14.29 log CFU/g in beef meat inoculated
meat and the redness is preferred by consumers. with 7, 8 and 9 log CFU/g, respectively, after 10 days of storage in the
refrigerated conditions. The growth of LAB is desirable from at least
3.4. Microbiological analysis two standpoints namely public health (control of pathogenic bacteria)
and economic matters (efficiency in sausage manufacture) (Commission
The relationship between log CFU/ml and OD for L. plantarum TN8 Regulation N° 2073/, 2005).
is shown in Fig. 1. The bacterial cells showed almost a linear re-
lationship represented by linear regression line with 3.4.2. Psychrotrophic counts (PTC)
Y = 0.902× + 7.694. This relation was used to estimate the Fig. 2B showed a significant reduction in the PTC counts in the

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I. Trabelsi, et al. Meat Science 154 (2019) 29–36

Fig. 2. A. Growth of Lactic Acid Bacteria (LAB) in different beef sausages during
refrigerated storage. T1: Control without probiotic culture, T2: treatment with
L. plantarum inoculated at 107, T3: treatment with L. plantarum inoculated at
108 CFU/g, T4: treatment with L. plantarum inoculated at 109 CFU/g.
Means ± SE. a, b, c, d: Different letters are significantly different (P < .05)
between formulations. A, B, C, D: Different capitals letters are significantly
different (P < .05) between storage days within the same formulation.
B. Growth of psychrotrophic count (PTC) in different beef sausages during re-
frigerated storage. T1: Control without probiotic culture, T2: treatment with L.
plantarum inoculated at 107, T3: treatment with L. plantarum inoculated at
108 CFU/g, T4: treatment with L. plantarum inoculated at 109 CFU/g.
Means ± SE. a, b, c, d: Different letters are significantly different (P < .05)
between formulations. A, B, C: Different capitals letters are significantly dif-
ferent (P < .05) between storage days within the same formulation.
C. Growth of Enterobacteriaceae counts in different beef sausages during re-
frigerated storage. T1: Control without probiotic culture, T2: treatment with L.
plantarum inoculated at 107, T3: treatment with L. plantarum inoculated at
108 CFU/g, T4: treatment with L. plantarum inoculated at 109 CFU/g.
Means ± SE. a, b, c, d: Different letters are significantly different (P < .05)
between formulations. A, B, C: Different capitals letters are significantly dif-
ferent (P < .05) between storage days within the same formulation.

4833, 2003). In fact, in our case, the shelf-life of treatments with L.

plantarum TN8 was at least 10 days, while the control samples started to
deteriorate after 8 days of storage. According to Aksu et al. (2005), the
use of probiotic strains was efficient to prevent psycrotrophic bacteria
growth in meat.

3.4.3. Enterobacteriaceae counts

As shown in Fig. 2C, Enterobacteriaceae counts were not detected in
all samples on the 4th day of storage. On day 7, these counts increased
significantly in all samples (P < .05). Nevertheless, it should be noted
that on this day, all Enterobacteriaceae counts of samples with probiotic
strain were significantly lower compared with control sample
(P < .05). Indeed, they recorded to 1.9, 1.8, 1.78 and 1.1 g CFU/g for
control and samples inoculated with 7, 8, and 9 log CFU/g, respectively.
Also, at the end of the storage, all Enterobacteriaceae counts of samples
with probiotic strains (T1, T2, and T3) were lower compared with those
made without probiotic strains. The Enterobacteriaceae counts are about
1.2 log CFU/ g in sample inoculated with 9 log CFU/g and held below
the detection limit which is 2 log10 CFU/g (ICMSF, 1986; ISO 4833,
2003). Our findings showed that the incorporation of probiotic strains
extends shelf-life of raw minced meat beef. Rubio et al. (2013) provided
that the effect of probiotic cultures in the inhibition of En-
terobacteriaceae growth was due to the production of organic acids. In
addition, Pereira et al. (2018) reported that the decrease of En-
terobacteriaceae counts may be attributed to presence of probiotic
strains that may be exerting a protective role against these pathogenic
microorganisms.
Furthermore, the result of detection test of L. monocytogeness and
Salmonella spp. is negatively for all samples. Pereira et al. (2018) ob-
served an anti-listerial effect of probiotic strains incorporation. In fact,
these strains themselves demonstrated the antibacterial activity in situ
against the studied spoilage bacteria. All these data confirm that the
studied products are suitable for human consumption as recommended
by the standard (APHA, 1992).

3.5. Association of protein and lipid oxidation with texture profile and color
samples incorporated with probiotic bacteria L. plantarum TN8 com- parameters changes and samples of raw minced beef meat
pared to the control sample. On day 7 of storage, the inoculated meat
with 9, 8.7 log CFU/g of L. plantarum TN8 led to the PTC counts re- Multiple stepwise regression analyses were performed to evaluate
duction of 4.2, 5 and 5.9 log CFU/g, respectively. The PTC reduction is independent association between protein and lipid oxidation with dif-
significantly accompanied by an increase of the probiotic strain in- ferent parameters after 10 days of storage in a model including samples,
corporation in the raw minced beef meat (P < .05). On the other hand, hardness, chewiness, cohesiveness, springiness, adhesiveness, a*,b*,and
on the same day, PTC counts in control sample were above 6.8 log CFU/ L* as independent variables (Table 5).
g. In fact, when the PTC bacteria counts were above 6.7 for raw minced Samples, MetMb and cohesiveness were found to be independently
meat beef, the product was considered unsuitable for consumption (ISO associated with TBARS (P < .0001; P = .002 and P = .014

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I. Trabelsi, et al. Meat Science 154 (2019) 29–36

Table 5 Acknowledgment
Stepwise multiple linear regression analysis between lipid and protein oxida-
tion and color and texture parameters at 10 day of storage. This research was financially supported by the Tunisian Ministry of
Dependent variables Independent variables β P value Higher Education and Scientific Research (LRCBS05). The authors
gratefully acknowledge Chahia industry for providing raw rinced beef
TBARS samples −0.153 < 0.0001 meat. We would like to thank Prof. Hammadi ATTIA for texture ana-
R2 = 0.936 MetMb 0.014 0.002
lysis. The authors would like to express their sincere gratitude to Mr.
R2 adjusted = 0.923 Cohesiveness −0.687 0.014
Hardness 0.073 0.465 Kamel MAALOUL for her constructive proof reading and valuable lan-
Chewiness −0.104 0.605 guage polishing services.
Springiness −0.002 0.987
Adhesiveness −0.077 0.293
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