LWT - Food Science and Technology 154 (2022) 112867

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LWT
journal homepage: www.elsevier.com/locate/lwt

Effect of Salvia (Salvia officinalis) on the oxidative stability of

salmon hamburgers
Cintia Stefhany Ripke Ferreira a, Bruno Henrique Figueiredo Saqueti b,
Patrícia Daniele Silva dos Santos a, Jiuliane Martins da Silva b, Marcos Antônio Matiucci b,
Andresa Carla Feihrmann b, Jane Martha Graton Mikcha b, Oscar Oliveira Santos a, b, *
a
Departamento de Química, Universidade Estadual de Maringá (UEM), Campus Sede, 87020-000, Brazil
b
Programa de Pós-Graduação em Ciência de Alimentos, Universidade Estadual de Maringá (UEM), Campus Sede, 87020-000, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: Nowadays, in the food it is common market to develop healthier products aiming at health benefits. Among the
Lipid oxidation alternatives, there are products with the addition of aromatic herbs, since, throughout the storage period, they
Antioxidant assays enhance the preservation of the desirable properties of these foods by preventing/delaying oxidative processes.
TBARS
In this work the efficiency of three concentrations (0.50, 1.00, and 1.50%) of Salvia officinalis powder in salmon
Salvia officinalis L
hamburgers were investigated. The results showed that Salvia officinalis was able to stop the oxidation process of
the meat matrix under analysis, presenting a good antioxidant and antimicrobial potential under the conditions
of raw and grilled hamburgers. Therefore, through the analyzes performed, it was possible to predict that Salvia
officinalis is a good strategy for the food industry when it comes to preserving salmon meat for a long period of
storage, in this case being studied for 90 days.

1. Introduction (Fogaça & Sant’Ana, 2007). To prevent or delay recurrent oxidation, the
usefulness of natural antioxidants has been a technological strategy
The fish consumption promotes health benefits, due to the concen­ (Vujovic, Pejin, Djordjevic, Velickovic, & Tesevic, 2016; Đorđević et al.,
tration of important bioactive ingredients, such as: essential amino 2018), as they replace synthetic antioxidants (Rahman, Alam, Monir, &
acids, vitamins, minerals, and especially polyunsaturated fatty acids Ahmed, 2021) directly related to health risks, thus arousing the interest
(Atitallah et al., 2019), of which the salmon deserves being highlighted, of the food industry (Caleja, Barros, Antonio, Oliveira, & Ferreira, 2017;
a fish of the Salmonidae family (Maluly et al., 2019; Merlo et al., 2019). Mira-Sánchez, Castillo-Sánchez, & Morillas-Ruiz, 2020).
Harris, Fleming, and Kris-Etherton (2011), and Kromhout and de Among the class of natural antioxidants, aromatic herbs stand out.
Goede, (2014) describe the salmon meat as a relevant source of funda­ An example is the Salvia case (Salvia officinalis L.), which confers anti­
mental fatty acids such as docosahexaenoic acid (DHA) and eicosa­ fungal, antibacterial, antiviral, and antioxidant properties (Vosoughi,
pentaenoic acid (EPA), important in the prevention of cardiovascular Gomarian, Pirbalouti, Khaghani, & Malekpoor, 2018) due to the content
diseases. In the face of the high production of fish in captivity, the fil­ of phenolic compounds (Mekinić et al., 2019). In this way, its applica­
leting industry uses the fish pulp for the production of, for example, tion in food is interesting.
hamburgers. This adds value to this raw material. Although there are studies on the application of Salvia officinalis in
However, due to the high concentration of polyunsaturated fatty foods (Estévez, Ramírez, Ventanas, & Cava, 2007; Zhang, Lin, Leng,
acids, hamburgers are susceptible to lipid oxidation when in contact Huang, & Zhou, 2013), studies on the application of this herb in salmon
with oxygen, heat, or light, the main degradation process of these foods products are still scarce.
(García-Lomillo, Gonzalez-SanJose, Del Pino-García, Ortega-Heras, & In this context, this work aimed to develop salmon burgers with
Muñiz-Rodríguez, 2017; Mizi et al., 2019). Salvia officinalis added in different concentrations (0.50, 1.00, and
The oxidation interferes with the sensory (Jacobsen, 2018) and 1.50%) to promote a healthier product option for consumers. In addi­
nutritional properties of products, directly affecting their acceptability tion, color, pH, Water activity (Aw), lipid oxidation, fatty acids profile,

* Corresponding author. Food Science Graduate Program, State University of Maringá, Av. Colombo 5790, 87020-000, Maringá, Paraná, Brazil.
E-mail address: [email protected] (O.O. Santos).

https://doi.org/10.1016/j.lwt.2021.112867
Received 30 September 2021; Received in revised form 12 November 2021; Accepted 23 November 2021
Available online 24 November 2021
0023-6438/© 2021 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
C.S. Ripke Ferreira et al. LWT 154 (2022) 112867

antioxidant compounds, and microbiological parameters were evalu­ performed in triplicate at time 0. In this context, the induction point of
ated during 90 days of storage at − 18 ◦ C. each sample was obtained by the method of two tangents.

2. Materials and methods 2.5. Lipid oxidation (TBARS)

2.1. Preparation of power The lipid oxidation was determined under raw and grilled condi­
tions, measuring the substances reactive to 2-thiobarbituric acid in a
The dehydrated salvia leaves (Salvia officinalis) were purchased from time from 0 to 90 days with fortnightly intervals for the raw ones, and in
the local market in the city of Maringá/PR/Brazil. Then they were the grilled condition in the initial time. For the analysis, it was utilized
ground in a knife mill of the brand Marconi (MA630, Brazil) and sieved the methodology proposed by Raharjo, Sofos, and Schimidt (1992) with
in an 80 mesh sieve (particles smaller than 0.177 mm), resulting in a fine modifications (Wang, Pace, Dessai, Bovell-Benjamin, & Phillips, 2002).
powder that was packaged and stored at − 18 ◦ C until the experiments Initially, 5 g of quadruplicate sample were weighed and 0.5 mL of
were performed. di-terc-butyl-methyl phenol (BHT) was added in tubes. Afterward, 18 ml
of trichloroacetic acid (TCA) were inserted, and filtration was carried
2.2. Production of hamburgers out through filter paper (Whatman no. 3). Then, 2 mL of the filtrate were
added to 2 ml of 2-thiobarbituric acid reagent (TBA), and the solution
Fresh salmon meat and salt were purchased from the local market in was placed in a water bath at a temperature of 80 ◦ C for 40 min. Sub­
the city of Maringá/PR/Brazil. The salmon was ground in a blender sequently, samples were read at 531 nm in UV-VIS (Genesys 10-S,
(Walita, Philips, Brazil), and afterward, the hamburgers were prepared UV/Vis, USA). The results obtained were quantified using a standard
following a standard formulation: salt (2%), Salvia officinalis (0.5, 1.0, analytical curve (1.10–8 to 10.10–8 mol/mL) of tetra ethoxy propane
and 1.5%), and salmon. The hamburgers were molded using a manual (TEP) solution and expressed in mg of malondialdehyde (MDA) per kg of
molder 8 cm in diameter and 1.5 cm thick, with approximately 100 g sample. The analyses were performed every 15 days during the period
each, and after, they were vacuum-packed, and stored at − 18 ◦ C for from 0 to 90 days of storage for raw hamburgers and at the initial time
further analysis up to 90 days in the raw samples. A control without for grilled hamburgers.
Salvia officinalis was also prepared. We replicated the entire experiment
three times (n = 9). 2.6. Water activity and instrumental color
To carry out the analysis in the grilled hamburgers, the samples were
thawed at 8 ◦ C for 12 h and then roasted on an electric grill (Grill Perfect The water activity of the raw and grilled samples were determined at
Taste, Cadence, Brazil) for approximately 15 min on each side, until the room temperature (25 ◦ C), using the Aqualab 4 TE apparatus (Meter
central temperature reached 72 ◦ C, controlled through the use of a Group, USA). The instrumental color was measured in a colorimeter
skewer thermometer (Incoterm, Brazil) and cooled to 25 ◦ C for analysis. (Konica Minolta, CR-400, Japan). The equipment was calibrated using
the white calibration plate (L* = 85.79, a* = − 0.45, and b* = 3.98),
2.3. Antioxidant analysis by DPPH with D65 standard illuminant, 10◦ observer, and 8 mm aperture size.
Measurements were performed at three points on each side of the
The DPPH analysis was carried out on Salvia officinalis (power) and product, and the results were expressed according to the CIE system,
hamburgers, following the methodology described by Saqueti et al. consisting of L* (luminosity) a* (variation from red to green), and b*
(2021). An extraction solution was prepared, composed of 46.5% (variation from yellow to blue). The analyses were performed at 90 days
ethanol acidified until pH 2 with hydrochloric acid (HCl). It was added of storage in the raw hamburgers and at the initial time in the grilled
to one beaker ratio solvent/sample of 8.7 mL g− 1 and held in the ones.
extraction ultrasonic bath (ELMA, Elmasonic P, Brazil), working at 80
kHz frequency, 30 ◦ C, and 50-min time. The extract obtained was 2.7. pH analysis
filtered through Whatman No. 3 filter paper, and then packed in an
amber flask and stored in a freezer (− 18 ◦ C) until the analysis was The pH values of the hamburgers were determined using a digital pH
carried out. meter (DM-22, Digimed, Brazil) containing a correctly calibrated dril­
The antioxidant capacity of Salvia officinalis extracts and hamburger ling probe with pH 4.0 and 7.0 buffer solutions, respectively, through
formulations (raw and grilled) was evaluated by the DPPH radical direct readings. The analyses were performed during the range 0–90
scavenging assay as described by Boroski et al. (2011). The absorbance days of packaging in the raw products and at time 0 in the grilled ones.
reading was performed at the wavelength (λ) 517 nm in a UV-VIS
spectrophotometer (Genesys 10-S, UV/Vis, USA). For the calculation 2.8. Direct derivatization of fatty acids
of the antioxidant activity, a standard curve was used with Trolox
(0–0.3 mg/ml); to give calibration curve (y = − 0.003x + 0.6175) and The direct fatty acid methylation was based on the method proposed
R2 = 0.9927, the result was expressed as μMol Trolox of equivalent (TE) by Figueiredo et al. (2016), on the basis of which, in triplicate, 0.01 g of
per g− 1 of sample. The analysis was performed in triplicate. each hamburger was added into 10 cm test tubes; afterward, 2.0 mL of
sodium hydroxide solution (1.5 mol L− 1) in methanol. The mixture was
2.4. Technique for evaluating lipid oxidation by oxitest placed in an ultrasonic bath for 5 min and then 2.0 mL of sulfuric acid
(1.5 mol L− 1 in methanol) were inserted into the test tubes and taken
The analyzes of samples were performed according Claus et al. again to sonicate for 5.0 min. Furthermore, 1.0 mL of n-heptane and
(2015) and Verardo et al. (2013) in which lipid oxidation was assessed 500.0 μL of tricosanoic acid methyl ester (23:0) were added. The tubes
by Oxitest (Velp Scientifica, Usmate, Italy), which brings efficiency and were homogenized for 2 min on a vortex (Phoenix, Brazil), and centri­
advantages to solid samples since it uses the original form without prior fuged at 2000 rpm for 1 min, and the upper phase was finally collected
fat extraction (Verardo et al., 2013). Thus, the analysis took place in two for analysis by GC-FID.
separate oxidation chambers that were sealed after the addition of the
samples. The samples (approximately 15 g) were exposed to accelerated 2.9. Gas chromatography (GC-FID)
oxidation conditions (oxygen pressure and temperature, which were
588 kPa and 90 ◦ C with a purity of 99.9999%, respectively), in which the Chromatographic analysis was performed to obtain the FA profile of
pressure variation in the chamber was followed. Analyzes were fish samples. A gas chromatograph equipped with a Shimadzu GC-2010

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C.S. Ripke Ferreira et al. LWT 154 (2022) 112867

Plus flame ionization detector (GC-FID) was used. Samples were injected Table 1
in split/splitless mode using a Select FAME brand CP-7420 fused silica DPPH test and Oxitest method.
capillary column of 0.25 mm cyanopropyl film (stationary phase) and Samples Formulations (%) DPPH OXITEST
internal diameter, in addition to being 100.0 m long. The gases used μMol TE g− 1
of sample Time in hours
were: H2 with a flow of 1.2 mL min− 1, and N2 30.0 mL min− 1 (makeup RAW 0.0 6.80 ± 0.58 de 10:09 ± 0.05 c
gas). For FID, synthetic air was at a flow rate of 300.0 mL min− 1 and H2 0.5 5.63 ± 1.55 e 11:20 ± 0.32 b
at 30.0 mL min− 1. At the beginning of the analysis, the column tem­ 1.0 12.94 ± 0.93 c 11:45 ± 0.29 b
perature was 165 ◦ C in 18 min, where, to reach 235 ◦ C, a heating ramp of 1.5 18.20 ± 1,78 b 12:32 ± 0.09 a
GRILLED 0.0 5.33 ± 0.46 e 9.12 ± 0.12 d
4 ◦ C/min was used for 20 min. The analysis performed in triplicate 0.5 9.23 ± 0.34 d 10.00 ± 0.06 c
totaled a 30-min run with an injection volume of 1.0 μL. 1.0 20.34 ± 1.35 b 10.30 ± 0.09 c
The identification of FAMEs was conducted by comparing the 1.5 20.54 ± 1.16 b 11.02 ± 0.07 b
retention time of the retention time and the retention time of the stan­ Salvia officinalis – 71.61 ± 2.05 a –
dard (FAME Mix, C4–C24, Sigma-Aldrich). FA compositions were Results expressed as mean ± standard deviation, for analysis in three replicates
expressed in mass (mg g − 1 of the samples). The analyses were per­ (Day 0). Different letters in the same column indicate a significant difference
formed during the range 0–90 days in the raw ones and at time 0 in the between them (p < 0.05) for the Tukey Test.
grilled products.
that the adherence of the main Salvia officinalis antioxidants were
2.10. Direct electrospray infusion mass spectrometry (ESI-MS) transferred to the hamburgers, which may present benefits in the tech­
nological development of these products, being able to delay lipid
The identification of the antioxidant compounds presents in the ex­ oxidation and increasing their shelf life (Zhang et al., 2013).
tracts (prepared in section 2.3) of Salvia officinalis and in hamburgers The cooking process of the hamburgers was responsible for a
under their raw conditions used a direct infusion electrospray mass considerable increase in the antioxidant activity, which ranged from
spectrometer (ESI-MS XevoAcquity§R (Waters, Milford, MA, USA), 12.8 to 63.9%. This increase is justified by the thermal cooking process,
operating in negative mode. Spectra were obtained in the scanning which used a temperature of 180 ◦ C. At this temperature, the ham­
mode in the range of m/z from 100 to 700 Da, where for the infusion, 50 burgers undergo some modifications, such as the loss of water through
μL of the extract was dissolved in 950 μL of ultrapure water. Afterward, evaporation and consequently the compounds concentration, the Mail­
1 mL of the solution was transferred to vial and 20 μL of 1% formic acid lard reaction, and its reaction products, and the bioavailability of the
solution was added; therefore, the sample was infused at a flow rate of bioactive Salvia officinalis compounds, as high temperatures are
10 μL min− 1. The working conditions of the ionization source were as responsible for facilitating the release of phenols in plant tissues. From
follows: source temperature, 150 ◦ C; cone flow, 40 L h− 1; capillary these factors, it is understood that after cooking, hamburgers have
voltage, 3.06 kV; desolvation gas flow (N2), 400 L h− 1; desolvation higher antioxidant activities for the analysis in question (Fernández,
temperature, 350 ◦ C; and the gas flow cone, 30 L h − 1. Data acquisition Fogar, Doval, Romero, & Judis, 2016). In the grilled hamburger with the
was performed with MassLynx v 4.1 software. addition of Salvia officinalis at concentrations of 1.0 and 1.5%, there was
no significant difference (p > 0.05). In this case, the recommendation to
2.11. Microbiological analysis use 1.0% is necessary to obtain a product with maximum antioxidant
activity under these conditions and formulations.
Microbiological analyzes for coliforms at 45 ◦ C, Salmonella sp.,
coagulase-positive Staphylococcus aureus, coliforms, and sulfite reducing
3.2. Ability to retard oxidation by the oxitest method
Clostridia were performed according to Brazil (2019). The results were
expressed in the most probable number (MPN) for coliforms at 45 ◦ C,
Table 1 also describes that the Oxitest method proved to be effective
presence of Salmonella, and in colony-forming units per gram (CFU/g)
to compare the oxidation of formulated hamburgers at the initial anal­
for the other microorganisms. The analyses were performed on the 90th
ysis time. In this context, the hamburger without additive starts to
day of storage of the raw hamburgers.
oxidize in 10 h and 9 min, while adding 0.05% of Salvia officinalis delays
the oxidation to 11 h and 20 min (p < 0.05). For 1.00% the value does
2.12. Statistical analysis
not differ from the previous one, but when compared to 1.50%, it pre­
sents a significant difference (p < 0.05) of 1 h and 12 min. Another point
Data from all analyzes were submitted to Analysis of Variance
described in Table 1 shows that cooking was responsible for a difference
(ANOVA) and Tukey’s means comparison test (p < 0.05) using the R-
in antioxidant activity, ranging from 9.61 to 10.71%.
Studio software (version April 1, 1106, 2009–2021).

3. Results and discussion 3.3. Lipid oxidation (TBARS)

3.1. DPPH radical scavenging capability The lipid oxidation of the formulated hamburgers was evaluated by
determining the levels of TBARS expressed in mg MDA/kg of sample and
The DPPH assay was used to determine the antioxidant activity of are shown in Fig. 1 (raw) and 2 (grilled).
Salvia officinalis and hamburgers formulated with different concentra­ The MDA, which is the main secondary product of lipid oxidation,
tions of the herb that were analyzed immediately after preparation showed differences between the initial and final times of the analysis for
(Table 1). It was possible to observe that the Salvia officinalis presented all hamburgers. It was possible to see in Fig. 1 that for the control
an antioxidant activity of 71.61 ± 0.00 μMol TE g − 1 of sample. Its sample, the mean TBARS value increased from 0.49 to 1.24 mg MDA/kg
antioxidant activity is justified by the presence of bioactive compounds, over the storage time.
including phenols, such as carnosol, rosmanol, and rosmarinic acid, On the other hand, the treatments using Salvia officinalis (0.5, 1, and
which are the main and most relevant in the plant, acting as hydrogen 1.5%) showed lower values than the control, as well as they presented
donors to reactive species (Pavić, Jakovljević, Molnar, & Jok, 2019). The small levels of oxidation during the storage period at freezing temper­
addition of Salvia officinalis in gradual concentrations to the hamburgers ature, where the hamburger with the treatment of 1.50% presented from
was responsible for the gradual increase in its antioxidant activity, 0.09 to 0.27 mg MDA/kg, and the 0.00% burger reported greater
varying between 6.80 and 20.54 μMol TE g-1 of the sample. This suggests oxidation. Likewise, the addition of dehydrated Salvia officinalis at

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oxidation rate.

3.4. Water activity (Aw)

The Aw values are closely linked to the deterioration of food prod­

ucts and their reactions (Li, Zhu, Guo, Peng, & Zhou, 2011), and they are
shown in Fig. 3.
The results described in Fig. 3 indicated that all proposed formula­
tions remained between a range of 0.994 and 0.972 throughout the
storage time, and in the initial time, the 0.00%, 0.50%, 1.00%, and
1.50% hamburgers presented Aw values of 0.994, 0.976, 0.988, and
0.976, respectively, with significant differences between them (p <
0.05). On the other hand, at the end of the storage, Aw values were
0.984, 0.981, 0.977, and 0.974, following the same order. Possibly as the
added Salvia officinalis was powdered, it may have contributed to the
decrease in Aw.
Under grilled conditions, it was observed in Fig. 4 that the percent­
age of Salvia officinalis did not change the Aw values statistically be­
tween the four samples. However, when comparing the conditions (raw
Fig. 1. Lipid oxidation of raw hamburgers. and grilled), there was a significant difference (p < 0.05) between them,
showing that the Aw was lower after cooking.
concentrations of 0.05 and 1.00% decreases lipid oxidation and MDA
values when related to 0.00% due to its antioxidant characteristics. 3.5. Instrumental color
Therefore, it is possible to say that the greater the proportion of
Salvia officinalis, the lower the TBARS values observed throughout the Changes in the color of the outer surface of the hamburger samples at
analyzed period, which indicates less oxidation (p < 0.05). These results the beginning and end of storage and different Salvia officinalis con­
are in agreement with Tran et al. (2020) who added guava leaf extract in centrations are shown in Fig. 5.
fresh pork sausage and concluded that the extract was as efficient as the The L* value (brightness) of all hamburger samples did not differ (p
artificial antioxidant BHT in reducing lipid oxidation. Similarly, Zhang > 0.05), maintaining the same brightness perception between the same
et al. (2013), using different levels (0.05, 0.1, and 0.15%) of sausage samples at different storage times. Samples with different Salvia offici­
extract of Salvia officinalis, showed that the higher the addition of nalis concentrations had a reduction in the L* value proportionally with
extract, the lower the TBARS values. the increase in Salvia officinalis concentration, justified by the homog­
Regarding the lipid oxidation of the hamburgers (raw and grilled) enization process of the hamburger, releasing and uniformly distributing
shown in Fig. 2 during the period from 0 to 90 days of analysis for the the Salvia officinalis pigments.
raw products and at the initial time for the grilled products, it was The a* values (redness) of the hamburger samples decreased after 90
observed that when grilled, the hamburger has greater oxidation. days of storage, while the b* values (yellowing) increased. The re­
However, the TBARS values for both are within the acceptable value for ductions in a* values vary between 38.6% and 67.3%, the greatest
their consumption, which, according to Qiu and Chin (2021), establishes reduction being for hamburger samples with the addition of 1.50% of
2.5 mg of MDA/kg of the sample as the minimum value to produce Salvia officinalis. This reduction can be justified by the greater release of
undesirable sensory properties, such as rancidity. pigments during storage. When the value is close from zero, there is
In this context, when relating temperature application and the intermediation between red and green. For b*values, the increases in 90
TBARS assay, the results were in agreement with Wang, He, Gan, & Li days were between 9.4 and 29.2%. The yellowing of the samples
(2018) who report that, in general, lipid oxidation is a decreased concerning the addition of Salvia officinalis, that is, the control
temperature-dependent reaction, and the lower it is, the slower the sample (0.00%) had the highest value (30.87) and remained so during

Fig. 2. Lipid oxidation of raw and grilled hamburgers. Fig. 3. Water activity in raw hamburgers.

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cooking process are generated by the Maillard reaction, loss of water and
fat, and protein denaturation, which may mask some color changes
resulting from the formulations.

3.6. Effect of Salvia officinalis on pH and its changes during storage

The pH value of meat products is related to sensory properties, such

as juiciness, freshness, color, tenderness, among others, and its analysis
over time can help to understand the damage that occurs in food
matrices (Tamkutė et al., 2021). Thus, an analysis of the effect of Salvia
officinalis on the pH values of the products is shown in Figs. 7 and 8.
Fig. 7 shows that there was a decrease in pH values, with a significant
difference (p < 0.05) for the 0.00% sample during the 90 days. The
results also describe that for the other treatments, the addition of Salvia
officinalis reduced the pH value at a slower rate when compared to the
control product, showing that the pH values in all treatments, despite
having decreased over the days, differ from each other (p < 0.05).
According to some authors, the pH reduction during the storage of
meat products is due to the production of lactic acid by lactic acid
Fig. 4. Evaluation of Salvia officinalis power in hamburgers after cooking. bacteria (Sharma et al., 2017).
Furthermore, according to Fig. 7, it is possible to observe that there
the entire period evaluated compared to samples 0.50%, 0.10%, and was a significant difference (p < 0.05) between the 0.50% treatment
0.15%. Discoloration of meat products evaluated during refrigerated when compared to 1.00% and 1.50% in all periods, except for 90 days.
storage is common, caused by oxidative reactions in the product (Firuzi On the other hand, there was no significant difference (p < 0.05) be­
et al., 2019; Zhang et al., 2013). tween the 1.00% and 1.50% samples on days 30 and 45 of storage.
There was no significant difference for the L*, a*, and b* color pa­ In the case of grilled hamburgers (Fig. 8) the pH remained the same
rameters in the grilled products analyzed immediately after the cooking as for raw hamburgers, with no significant difference (p < 0.05) for
process (Fig. 6), showing agreement with the raw hamburgers evaluated samples with Salvia officinalis. Only the raw hamburger showed lower
in the interval from 0 to 90 days of storage. According to Selani et al. results after cooking (p < 0.05). Consequently, the changes that could
(2016), color changes in the raw samples are common when different cause damage to the hamburgers were not noticeable in either the
non-meat components are added, which can vary through the added grilled or the raw ones during the initial time of the analyses.
concentration; however, cooked samples do not show much difference, Our results are in agreement with Prado et al. (2019), who state that
as observed in the present work. The color changes caused by the pH is a meat quality indicator and must be between 5.6 and 6.2; thus, the

Fig. 5. Colorimetric analysis of samples before cooking.

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Fig. 6. Colorimetry analysis in samples after cooking.

Fig. 7. pH analysis over 90 days of storage.

Fig. 8. pH analysis in different treatments at initial time.
burgers of this study are considered suitable for consumption.
0.05) over the days; however, because they contain only single bonds
3.7. Analysis of fatty acids by gas chromatography when compared to polyunsaturated-chain FA (PUFAS) (double and tri­
ple bonds), they presented a reduction to a lesser extent, proving to be
The lipid oxidation of the hamburgers during the storage period from more stable.
0 to 90 days at biweekly intervals for the raw ones and at the initial time Furthermore, considering the involvement of antioxidant com­
for the grilled condition was confirmed by the significant changes (p < pounds in lipids, it was observed that the quantification of PUFAS
0.05) in the FA profiles during the analysis (Table 2). Nineteen fatty increased as the Salvia officinalis concentration increased between 0.050
acids have been identified, but only the main ones are described in and 1.00% samples; nonetheless, the higher concentration did not in­
Table 2. crease this quantified proportion (p < 0.05). Thus, the recommendation
For the saturated-chain FA (SFA), the results show a decrease (p < of 1.00% is necessary for the development of a more nutritious product

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Table 2
Major Fatty Acid Composition (mg g− 1) of salmon hamburger with different percentages of Salvia officinalis.
Composition FA Treatments Time (days)
(mg g− 1) %

0 0 15 30 45 60 75 90

Raw Grilled

14:00 0.00 2.55 ± 0.24a 2.42 ± 0.03b 2.29 ± 0.18e 2.31 ± 0.13ce 2.22 ± 0.12b 2.12 ± 0.14d 2.28 ± 0.09e 2.34 ± 0.12c
0.05 2.66 ± 0.23a 2.61 ± 0.02b 2.48 ± 0.14c 2.45 ± 0.18d 2.32 ± 0.14e 2.23 ± 0.12f 2.21 ± 0.35f 2.20 ± 0.46f
1.00 3.39 ± 0.11a 2.73 ± 0.05c 2.82 ± 0.07b 2.84 ± 0.26b 2.45 ± 0.09d 2.45 ± 0.09d 2.24 ± 0.30e 2.22 ± 0.18e
1.5 3.53 ± 0.54a 2.85 ± 0.04c 3.27 ± 0.32b 2.71 ± 0.10d 2.73 ± 0.27d 2.74 ± 0.25d 2.39 ± 0.24f 2.32 ± 0.16g
16:00 0.00 15.42 ± 0.41a 15.03 ± 0.28b 13.90 ± 0.27c 13.75 ± 0.02d 13.50 ± 0.31e 12.87 ± 0.13f 12.11 ± 1.06g 12.05 ± 0.67h
0.05 17.06 ± 0.74a 16.87 ± 0.27b 15.42 ± 0.40c 15.23 ± 0.62d 13.93 ± 0.46e 13.42 ± 0.45f 13.36 ± 0.39g 13.28 ± 1.08h
1.00 24.29 ± 2.44a 18.28 ± 0.13b 17.41 ± 0.09c 16.73 ± 0.55d 15.13 ± 0.42e 15.07 ± 0.34f 14.38 ± 0.90g 14.28 ± 0.47h
1.5 23.29 ± 0.06a 18.35 ± 0.03c 18.58 ± 0.59b 16.72 ± 0.40d 16.10 ± 0.82e 15.58 ± 0.55f 15.56 ± 0.55f 15.40 ± 0.17g
16:1 n-7 0.00 2.61 ± 0.14a 2.66 ± 0.05b 2.54 ± 0.17d 2.56 ± 0.13c 2.46 ± 0.11e 2.35 ± 0.14f 0.19 ± 0.01g 0.17 ± 0.01h
0.05 3.47 ± 0.45a 3.06 ± 0.07b 2.71 ± 0.07c 2.68 ± 0.10c 2.53 ± 0.08d 2.44 ± 0.04cd 2.23 ± 0.05e 2.21 ± 0.01f
1.00 4.11 ± 0.57a 3.17 ± 0.17b 3.11 ± 0.06c 3.03 ± 0.09d 2.70 ± 0.09e 2.69 ± 0.07f 1.00 ± 0.05g 0.25 ± 0.01h
1.5 3.64 ± 0.05a 3.26 ± 0.06b 3.37 ± 0.12c 2.98 ± 0.10d 2.92 ± 0.14e 2.82 ± 0.09f 2.60 ± 0.02g 1.25 ± 0.21h
18:1 n-9 0.00 55.17 ± 0.30a 49.02 ± 0.10b 45.81 ± 0.60c 46.33 ± 0.02d 44.49 ± 0.53e 42.44 ± 0.45f 44.03 ± 0.13g 38.34 ± 0.63h
0.05 66.08 ± 0.63a 65.16 ± 0.18a 50.58 ± 0.58b 50.06 ± 0.99b 47.25 ± 0.48c 45.50 ± 0.50c 45.56 ± 1.46c 45.42 ± 0.81c
1.00 69.95 ± 1.91a 67.98 ± 0.17b 57.08 ± 0.75c 54.27 ± 0.60d 49.68 ± 0.94e 49.51 ± 0.51f 46.93 ± 0.94g 41.01 ± 0.79h
1.5 76.99 ± 0.46a 69.08 ± 0.08b 60.29 ± 0.27c 54.91 ± 0.57d 52.23 ± 1.37e 52.32 ± 0.25f 50.49 ± 0.65g 49.29 ± 0.24h
18:1n-7 0.00 4.83 ± 0.22a 4.33 ± 0.41b 4.59 ± 0.31c 4.55 ± 0.34c 4.37 ± 0.35d 4.16 ± 0.27e 3.24 ± 0.01f 2.82 ± 0.07g
0.05 5.90 ± 0.35a 5.96 ± 0.23b 5.56 ± 0.03c 5.50 ± 0.68d 5.19 ± 0.04e 5.00 ± 0.04f 3.51 ± 0.14g 3.42 ± 0.03h
1.00 6.35 ± 0.03a 6.19 ± 0.05b 6.21 ± 0.61c 5.92 ± 0.45d 5.39 ± 0.40e 5.38 ± 0.44e 3.76 ± 0.15f 3.43 ± 0.13g
1.5 6.54 ± 0.79a 6.53 ± 0.01a 6.53 ± 0.45b 5.96 ± 0.49c 5.70 ± 0.51d 5.51 ± 0.43e 3.86 ± 0.06f 3.64 ± 0.05g
18:2 n-6 0.00 21.28 ± 0.06a 20.26 ± 0.09b 18.89 ± 0.78c 19.00 ± 0.39c 18.34 ± 0.34d 17.93 ± 0.52e 17.50 ± 0.30f 15.61 ± 0.56g
0.05 25.52 ± 0.33a 23.32 ± 0.33b 21.19 ± 0.37c 20.93 ± 0.68d 19.41 ± 0.39e 18.69 ± 0.34f 17.93 ± 0.43g 17.42 ± 0.93h
1.00 27.93 ± 2.08a 25.63 ± 0.25b 24.20 ± 0.29c 23.13 ± 0.03d 20.69 ± 0.40e 20.95 ± 0.62e 20.26 ± 0.30e 19.72 ± 0.40f
1.5 30.88 ± 0.71a 27.44 ± 0.28b 25.69 ± 0.73c 23.23 ± 0.71d 22.06 ± 0.57e 21.32 ± 0.21f 21.17 ± 0.46f 20.89 ± 0.38g
18:3 n-3 0.00 5.49 ± 0.15a 5.48 ± 0.12a 2.34 ± 0.03b 2.37 ± 0.07b 2.27 ± 0.05c 2.92 ± 0.05d 2.17 ± 0.06e 1.28 ± 0.13f
0.05 6.30 ± 0.49a 6.04 ± 0.43b 2.57 ± 0.02c 2.54 ± 0.02c 2.40 ± 0.02d 2.31 ± 0.03e 2.25 ± 0.38f 2.19 ± 0.34g
1.00 8.32 ± 0.24a 7.93 ± 0.06b 3.62 ± 0.57c 3.46 ± 0.38d 3.27 ± 0.45e 3.26 ± 0.45e 3.10 ± 0.06f 3.00 ± 0.12g
1.5 8.13 ± 0.28a 8.09 ± 0.04b 4.73 ± 0.40c 4.51 ± 0.50d 3.37 ± 0.39e 3.48 ± 0.36f 3.44 ± 0.21f 3.55 ± 0.03g
20:4n-6 (AA) 0.00 9.33 ± 0.07a 9.24 ± 0.08b 9.16 ± 0.51c 9.17 ± 0.34c 8.80 ± 0.69d 8.40 ± 0.59e 4.09 ± 0.01f 3.08 ± 0.01g
0.05 10.90 ± 0.24a 10.79 ± 0.42b 10.77 ± 1.99b 10.62 ± 1.81c 10.27 ± 0.27d 9.85 ± 0.26e 8.50 ± 0.03f 8.29 ± 0.23g
1.00 9.94 ± 0.64a 9.21 ± 0.03c 9.80 ± 0.23b 8.27 ± 0.47d 8.22 ± 0.25d 8.19 ± 0.26e 7.02 ± 0.15f 7.00 ± 0.06f
1.5 10.15 ± 0.42a 10.10 ± 0.13b 9.58 ± 0.56c 9.41 ± 0.30d 8.95 ± 0.31e 8.69 ± 0.42f 7.54 ± 0.02g 7.09 ± 0.48h
20:5n-3 (EPA) 0.00 7.61 ± 0.17a 7.30 ± 0.08b 6.57 ± 0.04c 6.60 ± 0.09d 6.50 ± 0.08e 6.38 ± 0.06f 5.86 ± 0.02g 5.74 ± 0.01h
0.05 7.48 ± 0.36a 7.45 ± 0.07a 7.35 ± 0.21b 7.17 ± 0.23c 6.58 ± 0.20d 6.42 ± 0.18e 6.35 ± 0.16f 6.25 ± 0.11g
1.00 8.90 ± 1.20a 8.66 ± 0.22b 7.52 ± 0.11c 7.77 ± 0.21d 7.31 ± 0.07e 7.30 ± 0.08e 6.98 ± 0.08f 6.95 ± 0.03g
1.5 7.71 ± 0.46a 7.62 ± 0.04b 7.66 ± 0.59c 7.45 ± 0.09d 7.49 ± 0.48e 7.14 ± 0.48f 7.12 ± 0.05f 6.88 ± 0.08g
22:6–3 (DHA) 0.00 1.52 ± 0.28a 1.47 ± 0.01b 1.22 ± 0.23c 1.24 ± 0.27c 1.19 ± 0.25d 1.13 ± 0.24e 1.14 ± 0.02e 0.79 ± 0.0 f
0.05 1.43 ± 0.07a 0.98 ± 0.01b 0.82 ± 0.08c 0.81 ± 0.07c 0.77 ± 0.08d 0.74 ± 0.07e 0.36 ± 0.06f 0.22 ± 0.01g
1.00 1.49 ± 0.05a 1.03 ± 0.03c 1.20 ± 0.75b 0.82 ± 0.07d 0.71 ± 0.05e 0.71 ± 0.05e 0.66 ± 0.09e 0.63 ± 0.18 f
1.5 1.59 ± 0.03a 1.33 ± 0.03b 1.34 ± 0.64b 1.28 ± 0.05c 1.15 ± 0.71d 1.11 ± 0.09e 0.84 ± 0.05f 0.78 ± 0.05g

Results expressed as mean ± standard deviation of triplicate. Day 0 grilled and 0–90 days of storage for raw condition. Values with different letters on the same line are
significantly different (p < 0.05) by Tukey’s test. Abbreviations for FA fatty acids, n = number of double bonds.

containing a good source of important FA, such as DHA, EPA, and AA. In officinalis extraction and the main compounds identified (Fig. 9b):
this line of thought, it was observed that the Salvia officinalis can pro­ Rosmarinic acid (m/z 359.14) (Fig. 9c), Carnosol (m/z 329.20), and
mote in fish meat a good source of lipids beneficial to human health that (Fig. 9d) Rosmanol (m/z 345.03).
are capable of preventing cardiovascular and gastrointestinal diseases Fig. 9 shows that rosmarinic acid is the major compound in the Salvia
(Brotas, Carvalho, & Pereira, 2020). officinalis extract; in addition, the secondary compounds rosmanol and
Furthermore, in accordance with Table 2, it is reported that cooking carnosol are obtained in lower intensity in this extract.
caused the loss of FA at high temperatures (p < 0.05), but even under The study on the different concentrations of the Salvia officinalis
these conditions, Salvia officinalis showed its power to preserve salmon substrate incorporated in raw hamburgers as a conservation method to
meat, presenting a greater quantification of FA when compared to the retard lipid oxidation was evaluated. The ESI-MS analysis was per­
control sample (0.00%). This can be explained by the fact that the herb’s formed to verify the variation in the intensities of the antioxidant
antioxidant compounds, due to the presence of temperature, did not compounds in the treatments; the results are described in Fig. 10. The
result in a significant loss of FA for human food, as is the case with error bars were not inserted as it would prevent the comparison between
0.00%. treatments; the standard deviations were less than 5% for all experi­
mental points.
3.8. Analysis by ESI-MS Fig. 10 shows that there was a significant increase in the intensity of
the antioxidant compounds due to the different concentrations of the
ESI-MS (negative mode) analyzes were performed (fingerprinting) Salvia officinalis substrate incorporated in the hamburger, especially
by direct infusion, to identify the main bioactive compounds present in between 0.5 and 1.0% concentrations, which can be used as a natural
the aqueous extract of Salvia officinalis at different concentrations antioxidant, bringing benefits for the consumer because it delays lipid
incorporated in the raw hamburger to verify which one had the greatest oxidation and consequently increases the shelf life of the product.
antioxidant capacity. Fig. 9a shows the “fingerprint” of the compounds
present in the aqueous extract obtained under the conditions of Salvia

7
C.S. Ripke Ferreira et al. LWT 154 (2022) 112867

Fig. 9. Spectra obtained by ESI-MS (negative mode) of the main bioactive compounds present and isolated in Salvia officinalis. (a) Fingerprint in the Salvia officinalis,
(b) Rosmarinic acid, (c) Carnosol, (d) Rosmanol.

8
C.S. Ripke Ferreira et al. LWT 154 (2022) 112867

Acknowledgment

The authors would like to thank the National Council for Science and
Technological Development (CNPq) and the Araucária Foundation for
Supporting Scientific, for the financial assistance and Technological
Development of the State of Paraná.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.

org/10.1016/j.lwt.2021.112867.

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