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Article

Evaluation of the Effect of Sage (Salvia officinalis L.) Preparations on Selected Quality Characteristics of Vacuum-Packed Chicken Meatballs Containing Mechanically Separated Meat

by
Aneta Cegiełka
1,
Marta Chmiel
1,*,
Elżbieta Hać-Szymańczuk
2 and
Dorota Pietrzak
1
1
Department of Food Technology and Assessment, Institute of Food Sciences, Warsaw University of Life Sciences, 166 Nowoursynowska Street, 02-787 Warsaw, Poland
2
Department of Biotechnology and Food Microbiology, Institute of Food Sciences, Warsaw University of Life Sciences, 166 Nowoursynowska Street, 02-787 Warsaw, Poland
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(24), 12890; https://doi.org/10.3390/app122412890
Submission received: 19 October 2022 / Revised: 6 December 2022 / Accepted: 14 December 2022 / Published: 15 December 2022
(This article belongs to the Special Issue Advances in Food and Food By-Products Analysis: Physical Characterization and Nutrient Analysis)
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Abstract

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The results of this study can help the manufacturers who produce ready-to-eat chicken meat products containing mechanically separated chicken meat in choosing the appropriate sage preparation to retard oxidative changes in lipids and bacterial growth.

Abstract

The aim of this study was to compare the effects of various forms of sage (Salvia officinalis L.) preparations on the quality characteristics of vacuum-packed chicken meatballs containing mechanically separated meat (MSM) from chickens during storage (+4 °C, 14 days). The meatballs tested in this study were prepared as follows: (1) without the addition of sage (control), (2) with 1.0% of dried sage (SD), (3) with 2.0% of 40% (v/v) sage ethanol extract (SEE40), (4) with 2.0% of 70% (v/v) sage ethanol extract (SEE70), and (5) with 0.1% of sage essential oil (SEO). The meatballs were assessed at weekly intervals for lipid oxidation, microbial quality, color parameters, selected organoleptic attributes, and other quality features. During storage, the lipid oxidation processes in the meatballs were slowed down by all the tested sage preparations, but the most effective slowdown was caused by sage ethanol extracts. On day 14, the values of thiobarbituric-acid-reactive substances determined in the SEE40 and SEE70 products (0.210 mg malondialdehyde [MDA]/kg and 0.233 mg MDA/kg, respectively) were significantly (p < 0.05) lower than that in the control (0.659 mg MDA/kg). Considering all the investigated microbial groups, the best antimicrobial activity was observed in the SEE70 and SEO products. On day 14, there were no significant (p > 0.05) changes in the aroma of the tested chicken meatballs, and only the SEO product showed significantly (p < 0.05) poorer appearance and color than the control. In conclusion, among the various sage preparations used in vacuum-packed chicken meatballs with MSM, SEE70 may be recommended to manufacturers.

1. Introduction

Ready-to-eat (RTE) meat products are gaining popularity in the food market worldwide. Being safe for the consumer, these products include all processed meat and poultry products that do not require additional preparation before consumption. Therefore, the major factors promoting the market growth of such meat products are that these products are convenient to use, or in other words, require simple preparation for consumption, and are available in wide varieties [1,2].
Poultry meat, including meat from chickens, is widely used as a raw material for the production of meat products referred to as RTE foods. It is characterized by good processing properties and mild flavor [2,3]. In particular, mechanically separated meat (MSM) is a profitable and attractive raw material for producing RTE meat products. MSM is also called “mechanically deboned meat” and “mechanically recovered meat” as these are obtained by applying external mechanical forces, such as pressure and/or shear force, to animal bones or parts of carcasses from which most of the adjacent muscle and fat tissue has previously been removed by hand or machine. However, in Europe, MSM is not widely used for the production of processed meat, and its use is limited to thermally processed meat products. MSM is preferred for industrial processes due to its low cost and the fact that it can serve as an additional source of protein in meat product formulations. Moreover, MSM preparation allows more efficient use of edible slaughter products by reducing the number of biological by-products that would need to be neutralized. However, it must be noted that this raw material is more susceptible to oxidative and microbial deterioration and its further processing may therefore have an impact on the quality and safety of meat products containing this kind of material in the recipe composition [4,5]. MSM from chickens is of nonuniform quality, and its quality as well as technological suitability is mostly determined by the production method. For example, “low-pressure MSM” is more similar to ground meat in structure and appearance due to the lower degree of damage to muscle cells compared to “high-pressure MSM” [6,7].
RTE meat products are preserved by cooling, freezing, or a combination of heat treatment, packaging, and cooling [1,8]. The deterioration in the quality of RTE and many other meat products observed over time is attributed to simultaneous chemical and microbiological changes [9]. Among the chemical processes, the stability of meat products during storage is significantly reduced by lipid oxidation, which is a multistage process and is influenced by many factors such as the recipe composition of the meat product, the degree of grinding meat and fat, and the use or absence of thermal processing [10]. The changes that deteriorate the quality and safety of various meat products can be limited by the use of antioxidants and preservatives. However, due to the distrust of consumers toward the usage of synthetic additives in food production, researchers are investigating the possibility of replacing them with plant-based ingredients with proven antioxidant and antibacterial properties. Ingredients such as dried and shredded plants, as well as essential oils or extracts obtained using various solvents, may be incorporated into meat products in a variety of forms. The possible applications of these substances to meat and meat products, as well as the mechanisms behind the preservative effect of bioactive compounds in essential oils and plant extracts obtained from various plants, have been discussed in earlier reviews [11,12,13]. It has been shown that plant-derived preparations can be applied to chicken meat and its products to improve their shelf life. Stojanović-Radić et al. [14] reported that the essential oils of basil and rosemary significantly inhibited microbiological spoilage of chicken meat stored at +4 °C and reduced the number of Salmonella cells in comparison to control samples. Sharma et al. [15] investigated the possibility of using essential oils obtained from various herbal plants to extend the shelf life of fresh chicken sausages that were packaged under aerobic conditions and stored at 4 ± 1 °C (20 days). In storage tests, the authors observed that clove oil had the best antioxidant effect in sausages and cassia essential oil was the most effective in preventing the growth of microorganisms. Can [16] investigated the effect of thyme essential oil on the shelf life of chicken meatballs during the refrigerated storage period (12 days, 4 ± 1 °C). Their study showed that thyme essential oil added to meat batter and applied to the surface of the product significantly slowed down lipid oxidation processes and the growth of many bacterial species, and thus extending the shelf life of meatballs. However, according to the author, an important criterion determining the usefulness of plant essential oils for meat products is the sensory acceptability of these products. Another study [17] proved that vacuum packaging material coated with rosemary oil could be added instead of rosemary essential oil in meat batter to extend the shelf life of refrigerated chicken meatballs. This type of packaging effectively inhibited microbial growth and lipid oxidation and improved the sensory properties of chicken meatballs. Shahbazi et al. [18] highlighted that Ziziphora clinopodioides essential oil can be used as a natural antimicrobial alternative to synthetic chemical preservatives in RTE meat products such as raw chicken meatballs. In their study, meatballs treated with different concentrations of this essential oil showed better microbiological, chemical, and organoleptic properties compared to the control product until the end of the storage period (12 days). Sorour et al. [19] attempted to compare the effect of thyme oil and liquid smoke produced from beech sawdust on the quality parameters, including microbiological, physicochemical, and sensory characteristics, of chicken meatballs stored at refrigerated temperature for 12 days.
Herbs and plant spices are a good source of compounds with antioxidant and antimicrobial effects for food. Sage (Salvia officinalis L.)—a species belonging to the Lamiaceae family—is one such valuable plant. Evidence confirms the use of sage by ancient humans for food and medicinal purposes. The wide applications of sage have been attributed to its unique properties including pleasant taste and preservative and therapeutic effects [20]. Research data show that sage contains many bioactive compounds, such as antioxidant [21,22] and antibacterial ones [23,24]. Study results demonstrate that sage preparations may allow for prolonging the storage stability of various meat products from pork [22,25,26,27], beef [28], and poultry [29,30]. Among the bioactive ingredients of sage, which have been proven to have both antioxidant and antibacterial properties, the following are mentioned: camphor, α-thujone, and eucalyptol [22,23,24]. Apart from this, sage preparations, such as water extract, essential oil, and ethanol extracts, have been successfully used in mechanically separated chicken meat that was vacuum-packed and stored in a frozen state (−18 °C, 9 months) [31] and in vacuum-packed mechanically deboned chicken meat stored at refrigerated temperature (4–6 °C, 14 days) [23].
The aim of the present work was to assess the effect of various sage preparations on quality parameters—including oxidation stability of lipids and microbial quality—of vacuum-packed chicken meatballs containing MSM from chickens during 14-day storage at +4 ± 1 °C. This study is one of its kind as no study has so far investigated the possibility of using various sage preparations obtained under laboratory conditions from the same raw material (dried sage leaves) to extend the storage stability and safety of this type of RTE meat products.
Novelty statement: Many previous studies have analyzed the use of sage essential oil and extracts to extend the shelf life of meat and meat products. In these studies, sage preparations were obtained from different batches of raw material, and their antibacterial and antioxidant activity was assessed by applying them to various meat products. This does not always allow comparing the results regarding the effectiveness of sage preparations obtained in individual studies. The present work compared the effectiveness of various sage preparations, which were obtained from the same raw material (dried sage leaves) under laboratory conditions, in inhibiting oxidation processes and bacterial growth in an RTE meat product. The tested meat product was chicken meatballs containing mechanically separated chicken meat, which was vacuum-packed and stored in refrigeration conditions (+4 °C, 14 days). The findings presented here would therefore enrich the knowledge about the properties of various sage preparations. The results of this study may also help manufacturers who produce RTE chicken meat products containing mechanically separated chicken meat to choose an appropriate sage preparation that can inhibit lipid oxidative changes and bacterial growth.

2. Materials and Methods

2.1. Preparation of Sage Ethanol Extracts and Essential Oil

The sage preparations (S. officinalis L.) used in this work were prepared by the authors in the laboratory. The raw material used to prepare all sage preparations was dried and crushed sage leaves which were purchased from a spice distributor (NANGA, Złotów, Poland). Following the manufacturer’s instructions, dried sage was produced in accordance with the in-house procedure, i.e., from plants grown in an area not exposed to environmental pollution and harvested when mature. Using an extraction method described by Cegiełka et al. [31], sage ethanol extracts were prepared using ethyl alcohol (96%, v/v, analytical purity; POCh, Gliwice, Poland). Briefly, the sage ethanol extracts were obtained by continuous extraction of sage leaves in a Soxhlet apparatus (Universal Extraction Systems B-811, Büchi Labortechnik AG, Flawil, Switzerland). To prepare each extract, 40 g of dried and crushed sage leaves was distributed into eight extraction thimbles. Ethyl alcohol of 40% (v/v) and 70% (v/v) concentrations was used as a solvent. Solutions of ethyl alcohol (96%, v/v) were prepared using ethyl alcohol and distilled water. The raw material in each thimble was extracted with 150 mL of the appropriate solvent for 15 cycles while the solvent boiling point was maintained constant. The portions obtained from each extract were combined, which resulted in approximately 550 mL of raw extracts. The raw extracts were filtered using a 180-μm thick filter paper (Whatman GE, LaboPlus Sp. z o. o., Warsaw, Poland). Subsequently, each extract was concentrated in a rotary evaporator (Model R-205, Büchi Labortechnik AG) until there was approximately 40 g of the extract left, corresponding to the weight of dried sage used to obtain the extract. Sage essential oil was obtained using the method described by Białecka-Floriańczyk and Włostowska [32], and the procedure by Cegiełka et al. [31]. Briefly, around 30 g of dried sage leaves was covered with 400 mL of water, and distilled in a Deryng apparatus (Simax Kavalierglas AS, Prague, Czech Republic) until essential oils were obtained. The chilled distillate was extracted four times with dichloromethane in a separatory funnel, and then water was removed by adding anhydrous magnesium sulfate. The obtained extract was concentrated in a rotary evaporator (Model R-205, Büchi Labortechnik AG). The solvent was evaporated at 30 °C and 540–560 hPa.

2.2. Production of Chicken Meatballs

The experimental material used was meatballs produced under laboratory conditions (semi-industrial scale). The following chilled raw materials were used for the production of meatballs: chicken thigh meat, MSM from chickens, and pork jowl, all of which were purchased from two Polish meat producers (Karczew, Poland and Suwałki, Poland). MSM from chickens was obtained using the desinewing technology. The raw material used for the production of MSM from chickens was chicken broilers’ femurs and scarps of thigh muscles, which remained after the removal of the muscle tissue from the broiler carcasses. The muscle tissue was separated from the connective tissue and sinews using a belt-drum separator (BAADER 605, Baader Food Processing Machinery, Trige, Denmark) which was a part of the equipment used for chicken meat processing in Suwałki (Poland). The raw materials were transported to the laboratory under refrigeration conditions.
All the meatball batters were prepared with the same basic recipe composition that included the following raw materials: MSM from chickens 50%, chicken thigh meat 35%, and pork jowl 15% (100% in total). Table salt and ground black pepper (Kamis, McCormick S.A., Stefanowo, Poland) were also added, each at 1.5% in relation to the weight of the meat batter. The following five types of meatballs were prepared for assessment: (1) without the addition of sage (control), (2) with 1.0% of dried sage (SD), (3) with 2.0% of 40% (v/v) sage ethanol extract (SEE40), (4) with 2.0% of 70% (v/v) sage ethanol extract (SEE70), and (5) with 0.1% of sage essential oil (SEO). The amount of sage preparation added was expressed in relation to the total weight of the meat batter, and was adopted based on the results of studies by other authors [33] and our own preliminary studies (results have not been published).
For the production of meat batters, the meat from chicken thighs and pork jowl was ground in a laboratory grinder (Mesko WN40, Mesko AGD Sp. z o.o., Skarżysko-Kamienna, Poland). Each of the raw materials was ground using a plate with a hole diameter of 4.5 mm. After grinding, the raw materials, i.e., chicken thigh meat and pork jowl, were mixed separately by hand, and each mixture was divided into five equal portions to prepare meat batters. The meatballs were formed by hand, and the weight of each was 40 ± 0.5 g. Then, the meatballs were baked in a combi oven (Rational Self Cooking Center, Rational, Rolling Meadows, IL, USA). The air temperature in the furnace chamber was set at 180 °C and the relative humidity at 10%, and hot air circulation was switched on. Baking was continued until the temperature in the center of the product reached 72 °C. After heat treatment, the chicken meatballs were cooled to ambient temperature (about 18 °C). Subsequently, the meatballs from each treatment were divided into three portions, and each portion was vacuum-packed using a packaging machine (Multivac C200, Multivac Sepp Haggenmüller GmbH & Co. KG, Wolfertschwerden, Germany). Multilayer plastic film bags (PE/PA, 75-μm thick; Despol Sp. z o.o., Piaseczno, Poland) were used for packaging. The vacuum-packed chicken meatballs were stored in refrigeration conditions (+4 ± 1 °C) for 14 days.
The experiment was performed thrice at 2-week intervals. The animal raw materials used were obtained from three different production batches.
The appearance of chicken meatballs before heat treatment (control) and after heat treatment (meatballs with the addition of sage preparations) are shown in Figures S1 and S2, respectively.

2.3. Assessment of Quality Features of Chicken Meatballs

On the production day, immediately after cooling the meatballs to ambient temperature, the thermal treatment yield and the content of basic chemical components of these products were assessed. After 1, 7, and 14 days of refrigerated storage, the chicken meatballs were assessed for the content of thiobarbituric-acid-reactive substances (TBARS), microbiological parameters, instrumental color parameters, and organoleptic properties.

2.3.1. Determination of Thermal Treatment Yield of Chicken Meatballs

The thermal treatment yield of chicken meatballs was determined in each treatment using a weight method with the following equation:
Thermal treatment yield (%) = [(weight of raw meatballs (g) − weight of thermally processed meatballs (g)) ÷ weight of raw meatballs (g)] × 100

2.3.2. Determination of Basic Chemical Components in Chicken Meatballs

The content of moisture, protein, and fat was determined in chicken meatballs in accordance with the PN-A-82109:2010 standard [34] using a near-infrared spectrometer (FoodScan™2, Foss Analytical A/S, Hillerød, Denmark). The spectrometer works in a spectrum range of 850–1500 nm and utilizes an artificial neural network for calibration. To prepare the samples for measurements, approximately 300 g of each treatment product was ground in a laboratory grinder (Mesko WN40, Mesko AGD Sp. z o. o.) through a plate with a hole diameter of 2.0 mm and then mixed thoroughly. The cuvette, which was part of the equipment, was filled with the ground meat product and placed in the measuring station. Measurement was performed automatically, and the results were read on a computer screen.

2.3.3. Determination of TBARS Content in Chicken Meatballs

To assess the progress of lipid oxidation processes in chicken meatballs, the TBARS value was determined using the extraction method described by Shahidi [35]. The absorbance (A) of the obtained filtrates was measured at 532 nm using a spectrophotometer (CampSpec M501, CampSpec Ltd., Leeds, UK). The reagent sample (blank) contained 5 mL of 10% (w/v) trichloroacetic acid (Sigma-Aldrich, Poznań, Poland) and 5 mL of 0.02 M thiobarbituric acid (Sigma-Aldrich, Poznań, Poland). The TBARS value was calculated by multiplying the absorbance (A) of a given sample by the conversion factor 3.6, and was expressed in milligrams of malondialdehyde (MDA) per kilogram of product.
The percent inhibition of lipid oxidation in chicken meatballs was calculated on days 1, 7, and 14 of storage according to the following equation:
Inhibition of lipid oxidation (%) = [(Cx − Tx) ÷ Tx] × 100,
where Cx is the amount of MDA in control meatballs on day x and Tx is the amount of MDA in the meatballs with sage preparation on day x.

2.3.4. Assessment of Microbiological Quality of Chicken Meatballs

The samples of chicken meatballs for microbiological analyses were prepared using the standard Polish procedure [36]. Briefly, the foil package containing the product was opened using a sterile scalpel and 20 g of the sample was taken with a sterile spoon. Then, the sample was mixed with 180 mL of sterile peptone water (bioMérieux Polska Sp.z o.o., Warsaw, Poland), and the first 10-fold dilution was obtained. The sample was homogenized in a stomacher blender (Lab Blender 400 Circular, Seward Ltd., Worthing, UK) for 1 min at a maximum speed and 18 °C. Serial tenfold dilutions were prepared by transferring 1 mL of the first dilution to 9 mL of sterile peptone water.
The microbiological quality of chicken meatballs was assessed by determining the number of various bacterial groups in RTE meat products subjected to heat treatment and stored at a chilled temperature. The total count of mesophilic aerobic microorganisms was determined based on the requirements of the PN-EN ISO 4833-1:2013-12 standard [37] using Plate Count Agar medium (BTL Sp. z o. o., Łódź, Poland). The count of psychrotrophic bacteria was determined in accordance with the PN-ISO 17410:2004 standard [38] using plate count agar medium (BTL Sp. z o. o.). The count of coliform bacteria was determined in accordance with the PN-ISO 4832:2007 standard [39] using Endo agar medium (BTL Sp. z o.o.). The count of Enterobacteriaceae was determined in accordance with the PN-EN ISO 21528-1:2017 standard [40] using violet red bile glucose agar medium (BTL Sp. z o.o.). The count of lactic acid bacteria (LAB) was determined in accordance with the PN-ISO 15214:2002 standard [41] using Man, Rogosa, and Sharpe medium (BTL Sp. z o.o.). In addition, the presence of Salmonella spp. was determined in 25 g of meatballs. For this, a 25 g sample was mixed with 225 mL of a sterile buffered peptone water solution (0.1%, w/v) for prepropagation of bacteria. Selective proliferation of bacteria was carried out using Rappaport-Vassiliadis Soya Broth medium (BTL Sp. z o.o.). Isolation of bacteria was performed using Hektoen and brilliant green agar medium (BGA; BTL Sp. z o.o.). The confirmation of colonies typical of Salmonella spp. and evaluation of suspect colonies were planned to be performed using the API 20E biochemical test system (bioMérieux, Craponne, France). However, due to the lack of growth of colonies characteristic of Salmonella spp. on Hektoen and BGA media, such identification of bacteria was not performed.
The bacterial counts were expressed as colony-forming units (CFU) per gram of product.
The appearance of Petri dishes with the cultures of bacteria determined in this work is shown in Figure S3.

2.3.5. Measurement of Color Parameters of Chicken Meatballs

The instrumental color parameters were measured on the cross-section of meatballs. The CIEL*a*b* color scale was used to measure the color parameters, which were expressed as L*, a*, and b*. The L* parameter refers to lightness, where 0 indicates black and 100 indicates white. The a* parameter indicates the level of greenness (−a*) or redness (+a*), while the b* parameter indicates the level of blueness (−b*) or yellowness (+b*). The measurements were carried out using a colorimeter (Konica Minolta CR-200, Minolta, Osaka, Japan) with the following settings: light source, D65; observer angle, 2°; and measuring head hole, 8 mm. Before each use, the colorimeter was calibrated against a white standard (L* = 99.18, a* = −0.07, and b* = −0.05). For each product, color was measured at five different points and the mean value was calculated.

2.3.6. Evaluation of Selected Organoleptic Attributes of Chicken Meatballs

The organoleptic properties of chicken meatballs were evaluated following general guidelines described by Baryłko-Pikielna and Matuszewska [42]. The evaluation was performed in a separate laboratory room dedicated to food quality assessment. The room temperature was around 18 °C, and white light was used for lighting. The assessment panel included eight members of both sexes who had knowledge of food analysis and technology. Prior to the first evaluation session, the panelists were briefed on the detailed rules of the organoleptic assessment of meatballs. Each time before the assessment, the meatballs were reheated in a combi oven (rational) until the temperature in the product center reached 60 °C. Then, the products were divided into quarters, placed on white plates, and served for evaluation. The samples of meat products were coded with random numbers of three digits. The panelists assessed the samples for appearance and color (the degree of color, uniformity of color, and the presence of dark spots) and aroma (perceptibility of aroma of baked chicken meat, perceptibility of odor deviations that could have resulted from the addition of sage preparations). Due to the COVID-19 pandemic, the taste and consistency of meat products were not evaluated.

2.3.7. Statistical Analysis

Statistica® v. 13.0 software (StatSoft Inc., Tulsa, OK, USA) was used for the statistical analysis of the results. One-way analysis of variance (ANOVA) was performed to identify the differences between the mean values. A significance level of α = 0.05 was adopted to assess the significance of differences between the mean values, and the Tukey HSD test was applied as a statistical test. Before the use of ANOVA, the normality of data was evaluated using the Shapiro–Wilk test. The homogeneity of variances for the datasets was confirmed using the Levene test.

3. Results and Discussion

3.1. Thermal Treatment Yield and Chemical Composition of Chicken Meatballs

The amount of weight loss in chicken meatballs during baking, which was expressed as the thermal treatment yield, did not significantly change (p > 0.05) due to the modifications of the recipe composition. The thermal treatment yield of the chicken meatballs was found to be 78.8–80.5% (Table 1).
In previous studies, the yield of RTE poultry meat products was determined by calculating the weight loss of these products after heat treatment. In the study by Zwolan et al. [43], the weight losses determined in poultry meatballs subjected to baking were on average 13.6–14.4%. The authors reported that these values were typical of products from minced meat which have been baked. In another study [44], it was confirmed that the cooking losses of meatballs depended on the method of heat treatment applied.
According to De Araújo et al. [45], the consumer perception of the quality of meat products is determined by their nutritional quality which is related to the chemical composition. These authors highlighted that it is very important to estimate the content of chemical compounds (basic nutrients) in various meat products and to disseminate this knowledge because negative stigmatization and beliefs with no scientific base greatly influence consumers’ attitudes toward meat consumption. In our opinion, this is a particularly important issue in relation to meat products containing MSM in the recipe composition.
In terms of the content of basic chemical components, there were no significant (p > 0.05) differences between chicken meatballs, regardless of the type of sage preparation included in the recipe composition (Table 1). The moisture content in chicken meatballs was found to be about 62.5%, and the content of basic nutrients, namely, protein and fat, was over 18% or about 18%, respectively.
The basic chemical composition of chicken meatballs determined in our study was similar to that found in other RTE products from chickens [30,43]. However, the meatballs assessed here contained slightly more fat and less moisture, which was most likely due to the use of MSM which is a raw material with a relatively high fat content. Studies have shown that the fat content in MSM from chickens may vary from 14.07% [46] to 20.41% [7].

3.2. Lipid Oxidation in Chicken Meatballs

In all types of tested chicken meatballs, the TBARS values determined during the entire storage period were low and remained below 0.659 mg MDA/kg (Figure 1).
Even at the end of the refrigerated storage period, the value of TBARS remained within 3 mg MDA/kg in each product, which—according to Selani et al. [47]—indicates that the product did not undergo excessive lipid oxidative changes. The mean values of the TBARS index in chicken products with various sage preparations, i.e., SD, SEE40, SEE70, and SEO, were lower than that in the control product, regardless of storage time. Compared to the control treatment, on day one, the lipid oxidation processes were significantly slowed down (p < 0.05) only in the SEE70 product, for which the value of inhibition against lipid oxidation was 72.9%. On the other hand, in SD, SEE40, and SEO products, the value of inhibition against lipid oxidation was 23.8%, 57.2%, and 57.7%, respectively. On day seven, the only significant (p < 0.05) difference in the progress of lipid oxidation processes was found between the SEE70 product and the control. Larger differences in TBARS values between individual meat products assessed in this study were found on day 14. On this day, the SD product had a significantly (p < 0.05) lower TBARS value (0.473 mg MDA/kg) in comparison to the control (0.659 mg MDA/kg), but a significantly (p < 0.05) higher TBARS value than the SEE40, SEE70, and SEO products. On day 14, the values of inhibition against lipid oxidation in SEE40, SEE70, and SEO meatballs were 68.1%, 64.6%, and 52.8%, respectively. The storage time had a negative influence on the oxidative stability of all chicken meatball products, as evidenced by the increase in the TBARS values (Figure 1). However, the lipid oxidation processes significantly progressed with the extension of the storage time only in the SEO product, and there were significant (p < 0.05) differences between days 1 and 7 of storage.
The results of this work showed that undesirable lipid oxidation processes in chicken meatballs containing MSM from chickens were retarded by all the tested sage preparations during storage (+4 °C, 14 days). The best antioxidant properties were shown by the 70% (v/v) sage ethanol extract; however, comparable effects were also observed for the 40% (v/v) sage ethanol extract and essential oil.
The findings of this study are consistent with the observations of Hać-Szymańczuk and Cegiełka [27], who assessed the effectiveness of various sage preparations (dried leaves, ethanol, and water extracts) in improving the oxidation resistance of a model product of minced pork. In addition, data prove that sage preparations can maintain the oxidative stability of basic raw materials used in the production of RTE chicken products, including MSM from chickens. It has been shown that compared to dried shredded sage the addition of sage essential oil or extract—water or ethanol—allows better protection of MSM from chickens obtained using high-pressure techniques against oxidative lipid changes [23]. Similarly, in the case of MSM from chickens obtained using low-pressure techniques and stored in a frozen state, the progress of lipid oxidation processes was very slow after 9 months of storage in samples with the addition of sage essential oil and sage ethanol (40%, v/v) extract [31]. In convenient poultry products, the oxidative changes of lipids can be retarded by using dried sage, i.e., dried and shredded leaves, as demonstrated in turkey meatballs [29]. Satisfactory preservation of convenient meat products containing dried shredded sage leaves has been observed with the application of a combination of high hydrostatic pressures [28]. Other studies have shown that lipid oxidation in chicken meatballs can be retarded with the addition of black cumin (Nigella sativa) [43], as well as water and ethanol extract from black cumin [48].
Nikmaram et al. [2] and Ni et al. [49] reported that the antioxidant activity of plant extracts can be attributed to various phenolic compounds and some secondary metabolites, which are structurally similar to well-known plant phenols with antioxidant potential. In food systems, phenolic compounds act by scavenging free radicals, chelating pro-oxidative metal ions, and quenching singlet oxygen. Similar sage preparations as in the present study, i.e., dried sage, sage ethanol extracts, and sage essential oil, were used in another work of Cegiełka et al. [31]. Based on the results of qualitative and quantitative analyses of the composition of various sage preparations, these authors concluded that the preparations differ with respect to the type and amount of biologically active compounds. In terms of quantity, the most abundant components in all sage extracts, i.e., water and ethanol, were rosmarinic, p-coumaric, and benzoic acids. The water extract from sage contained more than twice as much chlorogenic acid as the ethanol extracts. In sage essential oil, the quantitatively dominant compounds were camphor, linalool, R(+) limonene, and carvacrol. Based on their analyses, Đurović et al. [50] indicated that the dominant components in sage essential oils are camphor, eucalyptol, α-thujone, β-thujone, and borneol, which possess antioxidant properties.

3.3. Microbiological Quality of Chicken Meatballs

An important factor that determines the safety and storability of meat products is their microbiological quality. The production of RTE food products from poultry meat involves different technological operations. Despite the use of heat treatment, the microbial counts in the final product may be relatively high [51]. Because the microbiological quality of a meat product is primarily influenced by the condition of the raw materials, MSM as one of the raw materials will certainly favor the development of microflora [31].
In this study, both modifications to the recipe composition and the storage time had a significant (p < 0.05) effect on the microbiological quality of the tested chicken meatballs (Table 2).
In all samples of tested chicken meatballs, there was a growth of mesophilic aerobic microorganisms, regardless of the addition of the sage preparation (Table 2). On day one, the significantly (p < 0.05) highest number of these microorganisms was found in the SD meatballs (1.6 × 105 CFU/g), while the lowest number was in meatballs containing other sage preparations (from 2.1 × 103 CFU/g for SEO to 4.5 × 103 CFU/g for SEE40). The control meatballs had the highest number of mesophilic aerobic microorganisms on both days 7 and 14 (3.0 × 105 and 8.4 × 105 CFU/g, respectively), while the addition of sage preparations significantly (p < 0.05) reduced the number of these microorganisms in meat products. The best antimicrobial activity was observed in the SEE40 samples, with the lowest number of mesophilic aerobic microorganisms detected on day 14 (4.9 × 104 CFU/g). However, the number of mesophilic aerobic microorganisms in this product was comparable to that in chicken meatballs with the addition of other sage preparations—SEE70, SEO, and SD—which indicates no significant (p > 0.05) differences between these products. Regardless of the treatment, the number of mesophilic aerobic microorganisms on the last day of storage was significantly (p < 0.05) higher than on day one. However, the results suggest that the addition of sage preparations slowed down the growth of these microorganisms in chicken meatballs during 14-day storage.
Psychotrophic bacteria were present in all tested chicken meatballs, regardless of the modifications of the recipe composition (Table 2). On days one and seven, there were no significant differences in the number of these bacteria (p > 0.05) in meatballs with the addition of sage preparations. On day 14, the significantly (p < 0.05) highest number of psychrotrophic bacteria was found in the SD meatballs (3.5 × 105 CFU/g). The number of psychrotrophic bacteria significantly (p < 0.05) differed only in SEE70 and SEO treatments in terms of storage time. A significant (p < 0.05) increase in the number of psychrotrophic bacteria was observed in the SEE70 treatment between days 1 and 14 and in the SEO treatment between days 7 and 14. However, on day 14, both SEE70 and SEO meatballs had the lowest numbers of psychrotrophic bacteria (1.6 × 104 and 2.7 × 104 CFU/g, respectively).
The growth of coliform bacteria in chicken meatballs was significantly (p < 0.05) slowed down by the addition of sage preparations (Table 2), and this trend was maintained throughout the storage period. In the control treatment, the number of coliform bacteria ranged from 9.6 × 101 CFU/g (day 1) to 1.7 × 10 CFU/g (day 14), and in the products with sage preparation from 1.0 × 100 CFU/g (SEE40, SEE70, and SEO—on day one) up to 4.4 × 101 CFU/g (SE70—on day seven). Storage time did not significantly (p > 0.05) influence the number of coliform bacteria in any of the tested meatball treatments, although the highest number of these bacteria was found in each treatment on the last day of storage.
Sage preparations delayed the increase in the number of Enterobacteriaceae in chicken meatballs; however, compared to the control treatment, the significance of the differences in the number of these microorganisms depended on the type of sage preparation and the storage time of the meatballs (Table 2). SEE70 showed the highest efficiency in slowing down the growth and increase in the number of Enterobacteriaceae, which ranged from 5.0 × 100 CFU/g (day one) to 1.0 × 101 CFU/g (day seven). During storage, a significant (p < 0.05) increase in the number of Enterobacteriaceae was found only in the control meatballs between days 7 and 14. On the other hand, there were insignificant changes (p > 0.05) in the number of Enterobacteriaceae in chicken meatballs with the addition of various sage preparations, i.e., SD, SEE40, SEE70, and SEO, during storage. On day 14 of refrigerated storage, the number of Enterobacteriaceae in all types of chicken meatballs containing sage preparations was significantly (p < 0.05) lower compared to the control.
The sage preparations used in the study also showed antibacterial activity against enterococci (Table 2). The highest number of these microorganisms was observed in the control products on day seven (5.8 × 101 CFU/g). Among the sage preparations used, SEO and both ethanol extracts were the most effective in inhibiting the growth of enterococci. In the SEO meatballs, the number of enterococci remained at 1.0 × 100 CFU/g throughout the storage period. Storage time did not have a significant (p > 0.05) impact on the number of enterococci in any of the meatball treatments. Considering the type of sage preparation, dried sage (SD) was the least effective in inhibiting the growth of enterococci, with the number of these microorganisms in the SD product being close, i.e., insignificantly (p > 0.05) different, to that of the control product throughout the storage period.
Among the sage preparations added to the chicken meatballs, both ethanol extracts (SEE40 and SEE70) and sage essential oil (SEO) most effectively inhibited the growth of LAB. Throughout the storage period, i.e., on days 1, 7, and 14, the number of LAB was significantly (p < 0.05) lower in SEE40, SEE70, and SEO products than in the control. A significant (p < 0.05) increase in the number of LAB was observed between days 1 and 14 in the control, SD, and SEE40 products, and between days 7 and 14 in the SEO products.
Evaluation of the results of all microbial tests led to the assumption that sage preparations contributed to improving the safety of chicken meatballs containing MSM from chickens, which are baked, vacuum-packed, and refrigerated. Of the various sage preparations used in the study, both sage ethanol extracts and sage essential oil exhibited the best antimicrobial activity. According to the current state of knowledge, the antimicrobial properties of plant preparations are linked to the presence of different bioactive compounds. Sage has been known to have a high potential to inhibit the growth of microorganisms in meat products [13,52]. RTE poultry products are particularly susceptible to the growth of different microorganisms that cause spoilage such as psychrotrophs and LAB. As emphasized by Nikmaram et al. [2], due to the desirable properties of plant preparations, many researchers and producers are interested in using them in the preparation of convenient meat products.
In general, plant preparations have a very complex composition, and their antimicrobial activity cannot be attributed to a single chemical compound. On the contrary, their complex composition and antimicrobial activity can be due—similar to antioxidant activity—to a whole range of chemical compounds [13,24,52]. Studies on the chemical composition and antimicrobial properties of selected essential oils against selected bacterial strains have shown that sage oil contains the largest amounts of compounds such as camphor, linalool, R(+)limonene, and carvacrol. Regarding antimicrobial activity, sage essential oil at the tested concentration showed a growth-inhibitory effect (minimum inhibitory concentration) against most of the analyzed Gram-positive bacteria, while among Gram-negative bacteria only Proteus bacteria were susceptible to its activity. The bactericidal activity (minimum bactericidal concentration) of sage essential oil was noted only against some of the tested Gram-positive cocci.
Previous studies have qualitatively and quantitatively analyzed ethanol extracts from sage, similar to those used in this study [31]. The following acids were identified at the highest amounts in those extracts: rosemary acid (0.616–0.650 mg/mL), p-coumaric acid (0.256–0.258 mg/mL), and benzoic acid (0.070–0.072 mg/mL). Some other researchers have also identified the same acids as well as other bioactive compounds in sage preparations [28,53]. Furthermore, these authors determined the antimicrobial activity of sage essential oils against seven various microbial strains using the disc diffusion method. The obtained test results indicated that the antimicrobial activity of sage essential oils against the tested bacteria slightly varied depending on the method of preparation.
Another work [30] that analyzed the quality of chicken burgers showed that an aqueous sage extract showed antimicrobial potential. As in the present study, the growth inhibition efficiency of this extract differed between the studied bacterial groups. Hać-Szymańczuk and Cegiełka [27] demonstrated the antibacterial activity of various sage preparations, i.e., dried spice, water extract, and ethanol extract, in the model product of pork minced meat. As in our study, dried sage showed the weakest antimicrobial activity, which was evidenced by the higher count of psychrotrophic microorganisms from the Enterobacteriaceae family and enterococci compared to other products. The growth of most of the tested microorganisms was more effectively slowed down in model pork products during storage (10 days) due to the added sage extracts (both water and ethanol). The results of the study by Aziman et al. [54] revealed that the shelf life of chicken meat stored at refrigeration temperature can be prolonged by using antimicrobial packaging. These authors noted that overwrapping chicken breast muscles in a film with a coating containing sage extract slowed the growth of bacteria such as Escherichia coli, Salmonella typhimurium, and Staphylococcus aureus. According to the authors, the observed antimicrobial effect was due to the antimicrobial properties of the sage extracts or the overall activity of the formulated coatings.
As mentioned earlier, mechanically separated poultry meat is particularly susceptible to the growth of microflora. Sage preparations can be helpful in maintaining the microbiological quality of MSM from poultry. In the case of high-pressure MSM, which was vacuum-packed and stored (4–6 °C, 10 days), the growth of different bacterial groups was retarded by the application of sage essential oil, sage ethanol extract, and sage water extract [23]. Sage preparations such as water extract, ethanol extracts, and essential oil were also applied to the MSM from chickens obtained using a low-pressure technique. In this raw material, which was vacuum-packed and frozen for 9 months, a significant (p < 0.05) slowdown in the growth of mesophilic aerobic bacteria and psychrotrophic bacteria, coliforms, and Enterobacteriaceae was observed in comparison to the control sample, regardless of the type of sage preparation used. Sage essential oil showed the best antibacterial activity, although it did not differ significantly in this respect (p > 0.05) from other sage preparations. These findings emphasize that sage essential oil and ethanol extracts may help in extending the life of low-pressure MSM from chickens [31].

3.4. Color Parameters of Chicken Meatballs

The results of the color analysis showed that both sage preparations and storage time of meatballs caused relatively small but significant (p < 0.05) differences between the mean values of all color parameters, i.e., L*, a*, and b* (Table 3).
The storage of meatballs resulted in a significant (p < 0.05) decrease in the mean value of the L* parameter, regardless of the treatment. On day one, the significantly (p < 0.05) darkest color was observed in cross-section in the control product. Presumably, the darker color of the SD product could have been influenced by the “flecks” of dried sage leaves that could be seen on the surface of the cross-section of meatballs. On day 14, the mean value of L* was significantly (p < 0.05) highest in the SEO product and lowest in the SD product. When assessing the changes in the values of other color parameters (a* and b*), it was noted that only in the SEE40 product, the values of both redness and yellowness did not differ significantly (p > 0.05) during the 14-day storage. On day 1, the significantly (p < 0.05) highest redness value was determined in the control and SEO products, and on day 14 in the control product. Based on the mean values of the b* parameter, yellowness was found to be significantly (p < 0.05) highest in the SD treatment after 1 day of production. After 14 days of refrigerated storage, the lowest and statistically comparable values of the b* parameter were observed in the SEO, SEE40, and SD products. The influence of the application of various sage preparations on the color parameters of the chicken meatballs found in this study is unclear. However, the observed changes in the mean values of individual color parameters were not relatively high and most probably should not exclude the application of sage preparations in the manufacturing of RTE meat products from chickens.
According to Gál et al. [55], the color of RTE meat products depends mainly on the type and proportion of meat and fat in the recipe composition, as well as the type of nonmeat ingredients and the method of thermal treatment applied. The thermal treatment method has a lesser impact on the color of the final product as seen on the cross-section of meatballs than on the surface. As in this study, the influence on the color parameters of poultry meat and poultry products was of interest to other researchers who attempted various modifications of the recipe composition based on the application of ingredients obtained from plants. Zwolan et al. [43] noted clear trends in changes in the color parameters of poultry meatballs in their study, in which black cumin seeds were added to poultry meatballs. These authors found that the addition of black cumin led to a significant decrease (p < 0.05) in the L* and b* values, regardless of the time of storage of the vacuum-packed products at 4 °C. During the 14-day storage, the L* values of poultry meatballs gradually increased, while the a* and b* values decreased. Sohaib et al. [56] assessed the influence of directly added quercetin dihydrate in combination with α-tocopherol on the values of L*, a*, and b* parameters of chicken meat patties. The authors explained that the decrease in the redness values of patties during storage (7 days, cold store temperature) was due to the accumulation of metmyoglobin in the evaluated products. The b* values of patties also decreased during storage, but the differences in mean values were smaller than for the color parameter a*.
In the production of RTE chicken meat products, attempts have also been made to use plant waste materials, and to evaluate their impact on the quality of these products. Manzoor et al. [57] reported that the incorporation of 4% mango peel extract resulted in lower changes in the color parameters of chicken sausages compared to similar sausages, but with 2% or 6% of this extract. On the other hand, after 10 days of storage, the L* value of the sausages containing mango peel extract increased, while the a* value significantly decreased.

3.5. Organoleptic Quality of Chicken Meatballs

The mean scores determined in the evaluation of the organoleptic attributes of chicken meatballs were relatively high, i.e., not lower than 4.0 points on a 5-point scale (Table 4). However, chicken meatballs differed significantly (p < 0.05) in terms of both the analyzed attributes: appearance and color, and aroma. On days one and seven, there were no significant changes (p > 0.05) found in the appearance and color of chicken meatballs containing sage preparations. Only on the last day of storage, the SEO product, containing 0.1% of sage essential oil, was scored significantly (p < 0.05) lower for the external appearance and color than the control product.
As for the aroma, the scores significantly (p < 0.05) decreased with the passage of storage time only in the case of the control and SD products (Table 4). However, significant (p < 0.05) differences in aroma were only observed between days 1 and 14 of storage. In addition, between days one and seven of storage, the use of sage essential oil (SEO) and sage ethanol (70%, v/v) extract (SEE70) caused a significant (p < 0.05) difference in the aroma of chicken meatballs in comparison with the control product. The panelists stated that the “characteristic herbal aroma” of the two above-mentioned sage preparations could be slightly perceptible, which worsens the acceptability of the meatball aroma.
The results of our study suggest that the application of various sage preparations to chicken meatballs prepared using MSM from chickens did not cause any deterioration in the organoleptic attributes of the products such as external appearance, color, and aroma, which would result in their lack of acceptance. However, to obtain a product with fully satisfactory organoleptic properties, further research should be performed assessing the taste of the product and determining the appropriate amount of the preparation. The results of other studies [22] show that sage can modify the palatability of meat products.
Šojić et al. [22] analyzed the influence of various sage preparations on the quality of fresh pork sausage. These authors found that the addition of both sage essential oil and sage extract increased the scores given for the odor and flavor of sausages when the assessment was carried out on the day of production. Based on their study results, the authors reported that the acceptance of “new”, “characteristic” sensory properties resulting from the use of plant preparations should be treated as a factor determining consumer preferences for meat products. This means that individual perceptions of consumers regarding sensory quality may vary. Previous studies have indicated that the sensory characteristics of chicken meatballs may be influenced by preparations obtained not only from sage but also from other plants, such as rosemary [58]. Similar to our study, it was shown that the appearance and color of meatballs prepared with the addition of dried rosemary and with ethanol extracts were comparable to that of the control product; however, meatballs containing dried spice were scored the best for aroma and taste. The results of other studies suggest that the overall sensory desirability of poultry meatballs can be improved by adding black cumin to the meat batter [43]. Although lower scores were given for the overall desirability of meatballs over time, based on all sensory results, the authors concluded that black cumin does not significantly deteriorate the sensory attractiveness of these products to consumers.
The results of the organoleptic evaluation of chicken meatballs showed that during storage the scores given for appearance and color significantly decreased (p < 0.05) for SEE40, SEE70, and SEO products, while for the SD product the scores for aroma decreased. At this stage of the research, due to the relatively high scores given for each of the organoleptic attributes, the use of any sage preparation should not be excluded in the production of chicken meat products such as meatballs.

4. Conclusions

The study showed that sage preparations obtained under laboratory conditions exhibited antioxidant activity. During storage (+4 °C, 14 days) of chicken meatballs, which were baked and vacuum-packed, and contained MSM from chickens in the recipe, the best protection of lipids against oxidation was conferred by sage ethanol (70%, v/v) extract, sage ethanol (40%, v/v) extract, and sage essential oil. Sage ethanol (70%, v/v) extract and sage essential oil also exhibited good antimicrobial activity in chicken meatballs. None of the sage preparations used caused drastic deterioration of appearance and color, or aroma of meatballs during storage. However, to fully assess the organoleptic acceptance of this type of meat products, it is important to assess their taste or palatability. In light of the obtained results, the use of ethanol (70%, v/v) extract of sage can be particularly recommended to retard oxidative and microbiological changes in chicken meatballs.
The main strength of this study is that it demonstrated an improvement in the safety and storage stability of an RTE chicken product containing mechanically separated chicken meat in the recipe without the application of synthetic food additives. The study was carried out using sage preparations obtained in laboratory conditions. The obtained data may facilitate the development of “newer generation” preparations enriched with bioactive components derived from sage, dedicated to RTE meat products, which is planned in further research. An aqueous extract of sage may also be used to develop new sage preparations with improved properties. To assess the applicability of new sage preparations, it will be necessary to measure their antioxidant activity, for example, using a selected in vitro method.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app122412890/s1.

Author Contributions

Conceptualization, A.C. and E.H.-S.; methodology, A.C. and E.H.-S.; investigation, A.C., M.C. and E.H.-S.; data curation, M.C. and D.P.; writing—original draft preparation, A.C.; writing—review and editing, M.C., E.H.-S. and D.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 12890 g001 550
Figure 1. Changes in the TBARS value of chicken meatballs containing MSM from chickens during refrigerated storage (mean values; n = 3). Control, SD, SEE40, SEE70, and SEO: The symbols identifying the chicken meatball treatments are explained in the footnotes of Table 1. a,b Mean values marked with different letters differ significantly at p < 0.05—the differences refer to chicken meatball treatments on a given day of storage. A,B Mean values marked with different letters differ significantly at p < 0.05—the differences refer to days of storage of a given chicken meatball treatment.
Figure 1. Changes in the TBARS value of chicken meatballs containing MSM from chickens during refrigerated storage (mean values; n = 3). Control, SD, SEE40, SEE70, and SEO: The symbols identifying the chicken meatball treatments are explained in the footnotes of Table 1. a,b Mean values marked with different letters differ significantly at p < 0.05—the differences refer to chicken meatball treatments on a given day of storage. A,B Mean values marked with different letters differ significantly at p < 0.05—the differences refer to days of storage of a given chicken meatball treatment.
Applsci 12 12890 g001
Table
Table 1. Thermal treatment yield and chemical composition of chicken meatballs containing MSM from chickens (mean values ± standard deviation; n = 3).
Table 1. Thermal treatment yield and chemical composition of chicken meatballs containing MSM from chickens (mean values ± standard deviation; n = 3).
Quality FeatureTreatment 1
ControlSDSEE40SEE70SEO
Thermal treatment yield (%)80.5 a ± 1.1679.1 a ± 3.1179.0 a ± 0.5178.8 a ± 1.0079.0 a ± 2.47
Moisture content (%)62.4 a ± 2.5762.3 a ± 1.8362.7 a ± 0.6863.3 a ± 1.7062.7 a ± 0.32
Protein content (%)18.3 a ± 0.7918.5 a ± 0.2518.4 a ± 0.3018.4 a ± 0.3518.3 a ± 0.35
Fat content (%)18.0 a ± 3.3817.9 a ± 0.5617.8 a ± 2.4117.2 a ± 0.1017.8 a ± 1.93
1 Control: chicken meatballs without the addition of sage; SD: chicken meatballs with 1.0% of dried sage; SEE40: chicken meatballs with 2.0% of 40% (v/v) sage ethanol extract; SEE70: chicken meatballs with 2.0% of 70% (v/v) sage ethanol extract; SEO: chicken meatballs with 0.1% of sage essential oil. a Mean values in the row marked with the same letter do not differ significantly at p > 0.05.
Table
Table 2. Changes in the microbiological quality * of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 6).
Table 2. Changes in the microbiological quality * of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 6).
Time
(d)		Treatment 1
ControlSDSEE40SEE70SEO
Mesophilic Aerobic Microorganisms (CFU/g)
18.2 × 104 bA ± 1.7 × 1041.6 × 105 cAB ± 6.7 × 1044.5 × 103 aA ± 2.3 × 1032.2 × 104 aB ± 7.1× 1032.1 × 103 aA ± 8.0 × 102
73.0 × 105 bAB ± 1.1 × 1053.0 × 103 aA ± 2.0 × 1028.2 × 102 aA ± 5.1 × 1021.0 × 103 aA ± 4.0 × 1026.3 × 103 aA ± 4.3 × 103
148.4 × 105 bB ± 6.2 × 1052.6 × 105 aB ± 1.7 × 1054.9 × 104 aB ± 2.2 × 1041.1 × 105 aC ± 1.0 × 1041.4 × 105 aB ± 5.2 × 104
Psychrotrophic bacteria (CFU/g)
11.0 × 103 aA ± 2.6 × 1021.9 × 103 aA ± 1.4 × 1032.1 × 103 aA ± 1.9 × 1038.5 × 102 aA ± 7.0 × 1015.6 × 102 aA ± 4.0 × 102
74.9 × 103 aA ± 2.9 × 1031.7 × 105 aA ± 2.9 × 1052.3 × 104 aA ± 3.6 × 1041.0 × 104 aAB ± 9.4 × 1032.5 × 103 aA ± 1.6 × 103
141.0 × 105 aA ± 1.0 × 1053.5 × 105 bA ± 1.7 × 1053.1 × 104 aA ± 1.6 × 1041.6 × 104 aB ± 6.0 × 1032.7 × 104 aB ± 1.6 × 104
Coliform bacteria (CFU/g)
19.6 × 101 bA ± 8.4 × 1014.0 × 100 aA ± 5.0 × 1001.0 × 100 aA ± 0.0 × 1001.0 × 100 aA ± 0.0 × 1001.0 × 100 aA ± 0.0 × 100
71.6 × 102 bA ± 1.1 × 1021.0 × 100 aA ± 0.0 × 1001.0 × 100 aA ± 0.0 × 1004.4 × 101 aA ± 7.4 × 1011.1 × 101 aA ± 1.7 × 101
141.7 × 103 bA ± 1.7 × 1033.0 × 100 aA ± 2.0 × 1004.0 × 100 aA ± 3.0 × 1004.0 × 100 aA ± 5.0 × 1004.0 × 100 aA ± 3.0 × 100
Enterobacteriaceae (CFU/g)
12.9 × 101 abA ± 2.3 × 1014.6 × 101 bA ± 3.5 × 1011.0 × 101 abA ± 1.6 × 1015.0 × 100 aA ± 6.0 × 1001.0 × 101 abA ± 1.0 × 100
73.1 × 101 aA ± 8.0 × 1011.4 × 102 bA ± 9.7 × 1011.6 × 101 aA ± 1.7 × 1011.0 × 101 aA ± 8.0 × 1004.8 × 101 abA ± 6.2 × 101
141.1 × 102 bB ± 4.7 × 1013.8 × 101 aA ± 4.8 × 1014.0 × 100 aA ± 3.0 × 1008.0 × 100 aA ± 6.0 × 1004.0 × 100 aA ± 3.0 × 100
Enterococci (CFU/g)
12.3 × 101 bA ± 7.0 × 1002.1 × 101 bA ± 2.0 × 1012.0 × 100 aA ± 2.0 × 1001.0 × 100 aA ± 0.00 × 1001.0 × 100 aA ± 0.0 × 100
75.8 × 101 bA ± 3.1 × 1014.5 × 101 bA ± 2.7 × 1011.0 × 100 aA ± 0.0 × 1002.0 × 100 aA ± 2.0 × 1001.0 × 100 aA ± 0.0 × 100
144.8 × 101 cA ± 2.3 × 1013.9 × 101 bcA ± 3.9 × 1013.0 × 100 abA ± 3.0 × 1003.0 × 100 abA ± 4.0 × 1001.0 × 100 aA ± 0.0 × 100
LAB (CFU/g)
12.9 × 103 bA ± 9.5 × 1022.4 × 103 bA ± 2.5 ×1034.1× 102 aA ± 3.4 × 1024.9 × 102 aA ± 3.4 × 1023.0 × 102 aA ± 1.4 × 102
71.0 × 104 bAB ± 4.8 × 1035.1 × 103 abAB ± 3.4 ×1036.6 × 102 aAB ± 3.4 × 1022.0 × 103 aA ± 2.4 × 1034.6 × 102 aA ± 1.1 × 102
143.9 × 104 bB ± 2.5 × 1042.2 × 104 abB ± 1.4 ×1041.5 × 103 aB ± 6.4 × 1024.2 × 103 aA ± 3.3 × 1034.7 × 103 aB ± 3.3 × 103
* Salmonella spp. was not detected in any type of tested chicken meatballs. 1 The symbols identifying the chicken meatball treatments are explained in the footnotes of Table 1. a,b Mean values in the row marked with different letters differ significantly at p < 0.05 (different superscript letters indicate differences between treatments on a given day of storage). A,B Mean values in the column marked with different letters differ significantly at p < 0.05 (different superscript letters indicate the effect of the storage time of a given treatment on the examined quality characteristic).
Table
Table 3. Changes in the color parameters of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 3).
Table 3. Changes in the color parameters of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 3).
Time (d)Treatment 1
ControlSDSEE40SEE70SEO
L*
166.78 cC ± 0.5363.14 aB ± 0.7565.00 abB ± 0.1262.31 aA ± 0.0865.08 bA ± 0.62
766.02 dB ± 0.1861.90 aA ± 0.1865.52 cC ± 0.2863.20 bB ± 0.2066.10 dB ± 0.33
1464.24 dA ± 0.1561.65 aA ± 0.2763.53 cA ± 0.2163.04 bB ± 0.1764.97 eA ± 0.06
a*
15.80 cB ± 0.144.68 bB ± 0.134.17 aA ± 0.214.16 aA ± 0.295.53 cB ± 0.26
74.79 bA ± 0.084.07 aA ± 0.123.90 aA ± 0.143.78 aA ± 0.264.78 bA ± 0.26
145.74 cB ± 0.174.38 aAB ± 0.314.16 aA ± 0.194.78 bB ± 0.065.13 bAB ± 0.27
b*
18.30 aA ± 0.069.25 bC ± 0.628.29 aA ± 0.157.99 aB ± 0.168.48 aB ± 0.29
78.24 bA ± 0.107.47 aA ± 0.338.17 bA ± 0.287.26 aA ± 0.428.00 abA ± 0.08
148.81 cB ± 0.178.51 abcB ± 0.188.45 abA ± 0.318.72 bcC ± 0.168.23 aAB ± 0.10
1 The symbols identifying the chicken meatball treatments are explained in the footnotes of Table 1. a,b,c,d Mean values in the row marked with different letters differ significantly at p < 0.05 (different superscript letters indicate differences between treatments on a given day of storage). A,B,C Mean values in the column marked with different letters differ significantly at p < 0.05 (different superscript letters indicate the effect of the storage time of a given treatment on the examined quality characteristic).
Table
Table 4. Changes in selected organoleptic attributes of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 24).
Table 4. Changes in selected organoleptic attributes of chicken meatballs containing MSM from chickens during refrigerated storage (mean value ± standard deviation; n = 24).
Time
(d)		Treatment 1
ControlSDSEE40SEE70SEO
Appearance and Color (Points)
14.6 aA ± 0.214.5 aA ± 0.264.5 aC ± 0.064.5 aB ± 0.174.5 aB ± 0.12
74.4 aA ± 0.214.3 aA ± 0.214.2 aB ± 0.064.4 aAB ± 0.154.3 aB ± 0.06
144.3 bA ± 0.124.2 abA ± 0.064.1 abA ± 0.004.1 abA ± 0.174.0 aA ± 0.06
Aroma (points)
14.7 bB ± 0.174.6 abB ± 0.204.6 abA ± 0.214.4 abA ± 0.174.3 aA ± 0.10
74.6 bAB ± 0.064.4 abAB ± 0.064.5 bA ± 0.154.3 aA ± 0.124.2 aA ± 0.15
144.4 aA ± 0.124.2 aA ± 0.204.3 aA ± 0.124.3 aA ± 0.124.1 aA ± 0.06
1 The symbols identifying the chicken meatball treatments are explained in the footnotes of Table 1. a,b Mean values in the row marked with different letters differ significantly at p < 0.05 (different superscript letters indicate differences between treatments on a given day of storage). A,B,C Mean values in the column marked with different letters differ significantly at p < 0.05 (different superscript letters indicate the effect of the storage time of a given treatment on the examined quality characteristic).
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Cegiełka, A.; Chmiel, M.; Hać-Szymańczuk, E.; Pietrzak, D. Evaluation of the Effect of Sage (Salvia officinalis L.) Preparations on Selected Quality Characteristics of Vacuum-Packed Chicken Meatballs Containing Mechanically Separated Meat. Appl. Sci. 2022, 12, 12890. https://doi.org/10.3390/app122412890

AMA Style

Cegiełka A, Chmiel M, Hać-Szymańczuk E, Pietrzak D. Evaluation of the Effect of Sage (Salvia officinalis L.) Preparations on Selected Quality Characteristics of Vacuum-Packed Chicken Meatballs Containing Mechanically Separated Meat. Applied Sciences. 2022; 12(24):12890. https://doi.org/10.3390/app122412890

Chicago/Turabian Style

Cegiełka, Aneta, Marta Chmiel, Elżbieta Hać-Szymańczuk, and Dorota Pietrzak. 2022. "Evaluation of the Effect of Sage (Salvia officinalis L.) Preparations on Selected Quality Characteristics of Vacuum-Packed Chicken Meatballs Containing Mechanically Separated Meat" Applied Sciences 12, no. 24: 12890. https://doi.org/10.3390/app122412890

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