Ceylon gooseberry as an additive to improve the quality of meat pattiesAbstract
To enhance the antioxidant activity and quality of beef meat patties, and to make the best use of the wild fruit Ceylon gooseberry (CG), patties were prepared with varying concentrations of this fruit, from 0 to 3%. The physical-chemical, technological, and sensorial characteristics were evaluated over a seven-day storage period. The results showed a significant increase in radical scavenging activity for DPPH and ABTS assay in patties with CG. The addition of CG effectively reduced lipid oxidation and influenced the color, particularly the variables a* and b*. There was a reduction in hardness, accompanied by the lowest cooking loss, shrinkage rate, and diameter reduction in patties made with CG. Importantly, adding up to 3% CG can be done without compromising on the sensory quality of the product. The potential of CG to reform traditional patties into a healthier meat product is not only inspiring but also motivating, adding significant value to this wild fruit and the food industry at large.
Key words
ABTS; antioxidant; beef; DPPH; hamburgers; lipid oxidation
INTRODUCTION
Meat and meat derivates are products of animal origin consumed worldwide due to their sensorial characteristics, low price, ease of preparation, and many proteins with biological value (Alexandretti et al. 2019). Lipid oxidation is one of the main factors that limit the shelf life of meat and derivates, and it is influenced by temperature, oxygen, light, and microbial spoilage (Cardoso et al. 2022). Ground beef is more susceptible to lipid oxidation than whole-muscle beef cuts due to the disruption of muscle fiber membrane that leads to exposure of phospholipids to oxygen (Bellucci et al. 2022). Synthetic antioxidants are used for food preservation. However, due to carcinogenicity and toxicity effects found in compounds, studies on replacing synthetic antioxidants with natural ones are progressively growing (Soyuçok et al. 2024).
A wide variety of wild fruits are little known and commercially exploited. These fruits are rich in antioxidant substances as demonstrated in araçá, butiá, pitanga (Vinholes et al. 2017) and Ceylon gooseberry (Dovyalis hebecarpa) (Bochi et al. 2015b). Due to their antioxidant, anti-inflammatory, and antimicrobial activities, the popularity of these berries as a food additive has rapidly increased (Golovinskaia & Wang 2021).
Ceylon gooseberry is a fruit species in the Salicaceae family. Native to southern India and Sri Lanka, it is being cultivated as an exotic fruit in the southwestern regions of Brazil (Bochi et al. 2015a, Rotili et al. 2020). The fruit is globose has a diameter of 1-3 cm, with velvety purple skin covered with short velvety hairs and a juicy, acidic pulp that surrounds 9-12 pubescent seeds (Silva et al. 2022).
The fruit is rich in bioactive compounds, including anthocyanins in the purple skin and carotenoids in the yellow pulp, along with fibers, minerals such as calcium (Ca), phosphorus (P), and potassium (K), unsaturated fatty acids, and vitamins—primarily ascorbic acid (Perera et al. 2022, Bochi et al. 2015a, b).
Due to the high titratable acidity and low soluble solids content, fresh consumption is not appreciated and is instead commonly processed into jams or juices (Rotili et al. 2018, de Assis et al. 2018). However, the skin contains more than four times the antioxidant activity of the pulp, making the utilization of the whole fruit particularly valuable (Bochi et al. 2015a).
The potential of Ceylon gooseberry (CG) as a natural alternative to synthetic antioxidants in meat or meat products offers a hopeful and optimistic outlook for the future of food preservation (Fachinello et al. 2018, Abdel-Naeem et al. 2022). The incorporation of various natural ingredients in meat products can enhance qualities such as appearance, texture, juiciness, firmness, tenderness, aroma, and flavor. Additionally, it can help meet consumer expectations in an increasingly competitive and innovative driven market. In this way, the objective is to evaluate the antioxidant effects of CG in patties and the impact on the physical-chemical, technological and sensorial characteristics during storage time.
MATERIALS AND METHODS
Materials and reagents
Ceylon gooseberry (CG) fruits were from Marialva, PR, Brazil (23°28’42”S, 51°47’18”W, 673 m altitude), being harvested in April 2023. The fruits were sanitized, cut, and lyophilized (Alpha 1-4 LD plus Martin Christ, Osterode am Harz, Germany) and sieved to 48 mesh. The meat, fat, and salt were obtained from local businesses.
Folin-Ciocalteau, sodium carbonate, gallic acid, 2,2-azinobis radical (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), potassium persulfate and 2,2,-Diphenyl-
1-Picrylhydrazyl free radical (DPPH) were from Sigma Aldrich (Spruce Street, St Louis, USA). The other reagents used are analytical grades.
Characterization of Ceylon gooseberry
Physicochemical composition
The chemical composition of CG was determined through analyses of moisture, ash, crude protein, and lipids according to the Association of Official Analytical Chemists (AOAC 1995). The carbohydrate content was calculated by the difference between 100 and the sum of the percentages of moisture, protein, total lipids and ash. The dietary fibre analysis was carried out using a combination of enzymatic and gravimetric methods (AOAC 1995). The results were expressed on a dry matter basis.
The pH of fresh fruit was measured using a glass electrode pH meter (Tecnopon, mPA-210), while total soluble solids (°Brix) were determined with a digital refractometer (HI 96801 - Nusfalau, Romania). Titratable acidity (mg of citric acid 100 g-1 of fresh fruit) was assessed following AOAC (2005).
CG color was determined by direct reading of the powder using a colorimeter (Konica Minolta, CR400, Japan) and the reflectance of coordinates L* (+white; - black), a* (+red; -green) and b* (+yellow; -blue) using the CIELAB scale.
Pigments such as β-carotene, lycopene and total chlorophyll of CG samples were determined from an extract (1:100 m/v) with acetone: hexane (4:6). Absorbance was measured at 663, 645, 505, and 459 nm by spectrophotometer (Nagata & Yamashita 1992). Anthocyanin content was determined through the pH difference (Lee et al. 2005). The readings were taken on a spectrophotometer at wavelengths of 520 and 700 nm respectively. The results were expressed in mg cyanidin-3-glucoside equivalents (Cy3G) 100 g-1.
Determination of bioactive compounds
CG extracts were prepared with 100% methyl alcohol in 1:100 m/v for 10 min, followed by centrifugation for 15 min at 3000 rpm. Supernatants were recovered and used for analysis. Total phenolic compounds (TPC) were determined by the Folin-Ciocalteau method (Singleton & Rossi 1965). The CG methanolic extract was mixed with Folin-Ciocalteau and sodium carbonate, homogenized, and after 30 minutes, protected from light, the samples were read in a spectrophotometer at 725 nm. The absorbance results were compared with the gallic acid curve and expressed in mg gallic acid equivalent per gram of sample (mg GAE g-1).
Antioxidant activity
Antioxidant activity was carried out in the CG extract (1:100 v/v) from the capture of the radical 2,2’-azinobis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) (Re et al. 1999), free radical capture 2,2-Diphenyl-1-Picrylhydrazyl (DPPH) (Li et al. 2009) expressed in µM Trolox Equivalent g-1.
Technological Properties
Water absorption index (WAI) and water solubility index (WSI) were determined according to Anderson et al. (1970). Oil absorption capacity (OAC) was determined according to Lin et al. (1974). The results were expressed as percentages.
Elaboration of patties
Patties were made from increasing concentrations of CG (0% as a control, CG1: 1%, CG2: 2%, CG3: 3%). To prepare the patties, beef was processed in an electric grinder (B5509, Botini, SP, Brazil), chloride of sodium and CG in treatments (where required), followed by cold water. The pork fat was added and manually homogenized for 3 min.
Patties were molded into 50 g units, packed in a 0.08-micron polypropylene plastic bag, and stored under refrigeration at 4±1 °C for seven days. Patties were cooked on a grill until they reached an internal temperature of 98 °C to analyses hardness and color.
Proximal composition
The proximal composition of patties was determined through analyses of moisture, ash, protein, and lipids according to the Association of Official Analytical Chemists (AOAC, 1995). The carbohydrate content was calculated by difference. The results were expressed on the percentage of fresh matter.
Antioxidant activity
To determine the antioxidant activity of raw patties, methanolic extracts in a 1:5 ratio was prepared. As previously described, antioxidant activity was determined using ABTS and DPPH capture methods.
Lipid oxidation
Thiobarbituric acid reactive substances (TBARS) were quantified according to Fachinello et al. (2018). Extracts were prepared from the sample’s dilution (1:10 w/v) in an extracting solution (7.5% TCA, 0.1% gallic acid and 0.1% EDTA). The mixture was centrifuged for 10 min at 3000 rpm. The supernatant was filtered and mixed (1:1 v/v) with TBARS solution (562.5 μM HCl, 15% TCA and 1% thiobarbituric acid) after was heated (100 °C for 15 min) and cooled for 5 min; the reading was in a spectrophotometer at 532 nm. Results were expressed as mg MDA kg-1 of patty.
Physicochemical characterization
pH was measured using a pH Meter (Simpla PH140, AKSO, RS, Brazil). Color was measured on raw and cooked patties using the CIELab system as described above. Hardness (Kg) was determined by Brookfield texture analyzer-CT III equipment (Engineering Laboratories, INC., Middleboro, MA, USA) in the following configurations: probe TA4/1000, a load of 3g and 1mm s-1 of test speed.
The weight of the patties determined cooking loss (PC%) before and after the cooking process and shrinkage (E%) according to El-Magoli et al. (1996). Diameter reduction (RD%) was performed with a digital calliper, considering three diameter measurements at different points (Seabra et al. 2002).
Sensorial Evaluation
Sensory tests of acceptance, purchase intention, and order of preference (Meilgaard et al. 1999) were carried out by 75 untrained consumers in the Food Technology Laboratory at the University of Maringá, Maringá, PR, Brazil. Participants assessed the acceptability of cooked patties samples (2 × 2 cm), which were randomly served immediately after preparation at 50 °C. The patties were evaluated by taste, color, texture, aroma, and general appearance through an acceptance test using a nine-point semi-structured hedonic scale ranging from 1 point = extremely disliked to 9 points = extremely liked (Project approved by the Ethic committee: protocol no. 61258616.3.0000.0104; certificate approval code 1.844.259).
Statistical Analysis
The results obtained were subjected to analysis of variance using the SISVAR 5.6 statistical program (UFLA, MG, Brazil). Means and standard deviations were calculated for each variable. When differences were statistically significant, Tukey’s test was used with a significant level of 5%. The experiment was repeated three times, and the analyses were performed on three different patties of each treatment.
RESULTS
Characterization of Ceylon gooseberry
Table II presents the characterization of CG fruits. Carbohydrates are the predominant macronutrient (76.37 % dry matter), followed by dietary fiber (28.70 % dry matter), proteins (7.55 % dry matter) and a low lipid content (0.92 % dry matter). CG exhibits high acidity and a low pH (3.13 mg citric acid 100 g-1 and 2.98 respectively). The SS/AT ratio was 3.80. The phenolic compound found in CG was 9.21 mg GAE g-1. The capacity of radical scavenging showed 10.08 µM TE g-1 for DPPH and 23.13 µM TE g-1 for ABTS respectively. The color of CG tends to be red and yellow. The content of anthocyanins was 288 mg CY-3g 100 g-1.
The technological properties of CG revealed a high water absorption index (WAI) of 399.79 and an oil absorption capacity (OAC) of 227.22, accompanied by a relatively low water solubility index (WSI) of 12.35%.
Characterization of patties
Table III presents the proximal composition of patties formulated with different percentages of Ceylon gooseberry (CG). The incorporation of Ceylon gooseberry in patties increases moisture and carbohydrate content while reducing fat. The level of ash tends to increase while the proteins remain relatively unchanged.
Antioxidant activity, lipid oxidation and pH of raw patties made with Ceylon gooseberry are present in Table IV. ABTS and DPPH radicals scavenging increased antioxidant activity, which was accompanied by increased CG inclusion in the patties. Regarding storage time, antioxidant activity decreased for all treatments from the fourth day of storage. The addition of CG reduced the production of malondialdehyde in patties, especially with 3% inclusion. The pH of raw patties made with CG was lower than the control and there was a reduction in storage time.
Antioxidant activity by ABTS and DPPH assay, lipid oxidation and pH of raw patties made with Ceylon gooseberry with up to 7 days of storage at 4 °C.
The inclusion of CG changes in brightness (L*), red (a*), and yellow (b*) values of raw and cooked patties (Table V). Patties with CG were significantly lower in hardness compared to the control, and a decreasing trend was observed with increasing levels of added CG (Table VI). Also, patties added with CG showed less loss due to cooking, a lower shrinkage rate, and a minor reduction in the diameter (Table VI). Through sensory analysis, all patties received scores close to 6 that means “like slightly” (Figure 1).
Color of raw and cooked patties made with Ceylon gooseberry with up to 7 days of storage at 4 °C.
Texture and cooking properties of Ceylon gooseberry patties stored for up to 7 days at 4°C.
Scores of preferences (%) according to the consumers preferences and purchase intention (n = 75) in the sensory analysis of patties made with Ceylon gooseberry.
DISCUSSION
Characterization of Ceylon gooseberry
Ceylon gooseberry (CG) is an exotic fruit introduced in Brazil, little known and commercially exploited. The determination of physical-chemical parameters is a tool that provides information on characteristics of fruit, which adds value and assists in its applicability in the food industry. The proximate composition showed that the major components identified in CG were carbohydrates (76.37 % dry matter or 13g 100 g-1 of fresh weight). These results correlate with Bochi et al. (2015a) who analyzed fresh CG fruits (9-13g 100 g-1 of FW).
CG contains also high levels of dietary fiber (28.70 % dry matter). Dietary fiber is a complex carbohydrate consisting of both soluble and insoluble fiber that the body cannot digest. However, it provides numerous health benefits, including lowering preprandial cholesterol and postprandial blood glucose levels, boosting gastrointestinal immunity, and promoting satiety (Jurevičiūtė et al. 2022).
The pH of the fruits was 2.98, which is similar to the values reported by Silva et al. (2011) (2.61) and Ayala-Silva et al. (2014) (2.44). The soluble solids content was 11.87 °Brix, a value lower than those reported by Ayala-Silva et al. (2014) (14.34 to 16.28 °Brix), Bochi et al. (2015a) (12.6 °Brix), and Silva et al. (2011) (12 °Brix).
Due to its high acidity, low soluble solids content, and the bitterness of the skin, this fruit is considered unsuitable for fresh consumption (Rotili et al. 2018, de Assis et al. 2018). However, it is appreciated when used in the preparation of jams, liqueur or juices (Rotili et al. 2020) and can be used in meat products.
Wild berries, such as CG, are rich in phenolic compounds such as phenolic acids, tannins, stilbenes, anthocyanins, and flavonoids (Perera et al. 2022). The TPC value found in this study (9.21 mg GAE g-1) is above those by Perera et al. (2022) (6.77 mg GAE g-1) and Silva et al. (2022) (4.31 and 2.55 mg GAE g-1 found in pulp and peel respectively) (Table II). The differences can be explained by genetic factors, fruit maturation, environmental and climatic conditions, drying, extraction, storage techniques, and type of analysis performed (Rojas-Ocampo et al. 2021, Fathy et al. 2023).
Many phenolic compounds exhibit strong antioxidant properties (Bochi et al. 2015a) functioning by scavenging free radicals, donating hydrogen, and chelating metal cations (Tian et al. 2018). According to Bochi et al. (2015b), the major classes of phenolic compounds found in CG include flavonols, hydroxycinnamic acids, hydroxybenzoic acids, and flavanols. Additionally, glycosylated anthocyanins, such as delphinidin-3-rutinoside and cyanidin-3-rutinoside, are the predominant anthocyanins present in this fruit.
Anthocyanins, the primary class of phenolic compounds, are responsible for the red-to-purple coloration and the high appeal of wild berries (Bochi et al. 2015b). In this study, the anthocyanin content (288 mg 100 g-1) was higher than that reported by Silva et al. (2022) in CG peel (94.13 mg 100 g-1). Anthocyanins act as antioxidants by neutralizing reactive radical species through the transfer of a single electron or the removal of a hydrogen atom from phenolic groups (Golovinskaia & Wang 2021, Enaru et al. 2021).
The phenolic compounds in berries are biologically active and promote health benefits, including antihyperlipidemic, antihypertensive, anti-proliferative, anti-inflammatory, antibacterial, and antiviral effects (Golovinskaia & Wang 2021). Phenolic compounds can also be used in foods to inhibit lipid peroxidation and extend shelf life. These findings suggest that CG can be used as a natural antioxidant and food dye, offering potential benefits for both food and health applications.
Analyses of technological properties, such as water holding capacity (WHC), water absorption capacity (WAC), and oil absorption capacity (OAC) measure the interaction between water and oil molecules, are linked to the soluble and insoluble fractions of fibers and proteins (Barbosa-Martín et al. 2016). The WAI serves as an indicator of a flour’s capacity to absorb water and swell, which is essential for achieving desirable consistency in food systems, improving yield, and enhancing texture and body in the final product (Choi et al. 2012, Iwe et al. 2016). In this way, the CG showed almost 400% of WAI making it promising for application in food matrices, such as patties, as well as in enhancing the texture and consistency of products.
The CG showed low WSI (12.35%). Ingredients with higher WAI and lower WSI could be used in a product where the main concern is high viscosity (Bryant et al. 2001). Viscosity is an important quality criterion in emulsion technology, as it helps impart a specific texture to products such as processed meats, including sausages, mortadella, and salamis (Uzlaşır et al. 2020).
Regarding the OAC, CG indicated higher than 200%. The ability of food products to absorb oil contributes significantly to a pleasant mouthfeel and effective flavor retention, making it an essential attribute in food formulations (Iwe et al. 2016).
In summary, CG has proven to be a valuable ingredient or additive for the food industry. While the fruit’s characteristics limit its fresh consumption, its functional and technological properties show significant potential for application in food matrices.
Characterization of patties
The incorporation of CG in patties affected the levels of moisture, fat, and carbohydrates. The higher carbohydrate content in the fruit, combined with its greater water absorption capacity, contributed to these changes. However, all formulations comply with Brazilian regulations for hamburgers, which set a maximum fat content of 25%, a minimum protein content of 15%, and a maximum total carbohydrate content of 3% (Ordinance SDA No. 724, of December 23, 2022). CG presents several bioactive compounds that exhibit antioxidant activity. The aromatic ring of phenolic compounds has a free hydroxyl group that allows them to eliminate peroxyl radicals and form a stable final product to avoid further lipid oxidation (Abdel-Naeem et al. 2022). Several studies point to an increase in the antioxidant activity of meat products from adding natural ingredients aiming inhibition of lipid peroxidation, such as grape seed extracts to ground meat, propolis ethanol extract in beef and pork patties, malt bagasse and goji berry in patties (Amin & Edris 2017, Cardoso et al. 2022, Saraiva et al. 2019, Vargas-Sánchez et al. 2019).
The TBARS (thiobarbituric acid reactive substances) values (mg malondialdehyde kg-1) are frequently used to measure the oxidative rancidity that occurs in meat products during storage (Fathy et al. 2023). The oxidation leads to lipids, pigments and protein degradation in meat and meat products (Cardoso et al. 2022). Strategies for delaying lipid oxidation and microbial spoilage are significant for the extension of the shelf life of this product (Amin & Edris 2017). In this way, the bioactive compounds present in CG can reduce the propagation of oxidative reactions. The phenolic compounds present in blueberries have the ability to scavenge oxygen radicals and inhibit lipid oxidation in burgers (Fathy et al. 2023).
One of the key quality parameters of meat products is its pH value, which plays a crucial role in determining other quality attributes, such as color changes, water-holding capacity, texture, and shelf life (Tian et al. 2022). The treatments with CG addition and the storage period significantly affected the patties’ pH. The pH value of patties CG added was lower when compared to the control, due mainly to phenolic acids and ascorbic acid presence. There was a reduction in pH from the fourth day of storage for all treatments, probably due to the production of lactic acid and other acids (Vergara et al. 2020). Similar behavior was obtained in low-fat hamburgers with malt bagasse (Saraiva et al. 2019), with ginseng extract (Soyuçok et al. 2024) and with grape seed extract in minced beef (Amin & Edris 2017).
Color is one of the most critical attributes of meat quality. In meat products, the oxidation of heme proteins leads to color deterioration during storage. Temperature, pH, oxygen availability, and lipid oxidation are the most significant factors affecting myoglobin oxidation and, consequently, meat color stability (Hoa et al. 2021). The reduction of luminosity (control), coupled with the decline of a* and b* values, in raw patties, evidences the impact of these parameters throughout storage.
The inclusion of CG affected the brightness (L*), red (a*), and yellow (b*) values of both raw and cooked patties (Table IV). CG contains anthocyanins and carotenoids, which impart a purplish hue to the meat without affecting its brightness. Color is a crucial sensory attribute that influences consumer acceptance. While CG alters the meat’s color (Table IV), it does not impact the sensory analysis results (Figure 1).
Cooked patties exhibited the combined effects of CG inclusion and storage time on color parameters. While CG decreased luminosity and redness, storage time primarily affected luminosity. Cooking significantly altered color parameters due to the Maillard reaction, protein denaturation, and the loss of water and fat (Sayas-Barberá et al. 2020).
The hardness of patties with up to 7 days of storage at 4 °C is described in Table V. The high carbohydrate content in CG fruit exhibits an affinity for water molecules (as shown by WAI), making it a gel with some characteristics similar to fat, contributing to lower patty hardness. Beef patties that are less gummy, not hard, less springy and cohesive, and easy to chew are preferred by consumers (Akwetey & Knipe 2012). Also, the inclusion of CG promotes less loss due to cooking, lower shrinkage rate, and a minor reduction in the diameter concomitant with the increase in the concentration of the added fruit, meaning that the CG allows the maintenance of the shape and size of the patties during cooking. The physicochemical properties of the carbohydrates in CG may influence the interactions between carbohydrates and proteins in meat and, thus, the water-holding capacity of meat products improving textural characteristics such as tenderness, juiciness, and cooking loss (Persson et al. 2004). These results agree with those found by Carvalho et al. (2017), using textured soy protein, collagen, maltodextrin, and their combinations in beef burgers and Akwetey & Knipe (2012), who used gari (precooked product obtained from cassava root) in beef burgers.
Through sensory evaluation (n = 75) of patties with varying concentrations of Ceylon gooseberry compared to a control (without the fruit), no significant differences were found in color, smell, texture, flavor, or overall acceptability. This suggests that Ceylon gooseberry does not impact consumer experience. On the hedonic scale, color received the lowest scores across all treatments. However, flavor scored between 6 (slightly liked) and 7 (moderately liked).
Similar results were obtained by Saraiva et al. (2019) (scores between 6-7) and Carvalho et al. (2017) (scores between 5.7-7). These results demonstrate that the CG as an additive in beef patties up to 3% did not significantly influence the sensory attributes while improving their nutritional properties.
The purchase intention evaluation revealed that patties with 1% Ceylon gooseberry (CG1) had the highest acceptance rate (49.33%), surpassing the control (41.33%) (Table VI). This suggests that a small addition of the fruit can enhance purchase intention. Conversely, rejection rates (“I would not buy”) were higher for patties with 2% and 3% Ceylon gooseberry (CG2 and CG3, both at 28%), while CG1 had the lowest rejection rate (13.33%).
In the ranking of preferences test, consumers ranked the samples in order of preference. CG1 emerged as the most preferred, with 36% of consumers selecting it as their top choice, while CG2 and CG3 were less favored compared to the control. Overall, the addition of 1% Ceylon gooseberry (CG1) enhanced product acceptance in both purchase intention and sensory preference. In contrast, higher concentrations (CG2 and CG3) appeared to reduce acceptance, possibly due to their impact on flavor or texture.
CONCLUSIONS
The use of Ceylon gooseberry in patties increased the anti-radical activity, although it does not result in less lipid oxidation. The color presented with less luminosity, less intensity of red, and more intense yellow. The CG improved the patties’ cooking properties and texture quality without compromising sensory quality, especially 1% CG. Ceylon gooseberry can be an alternative to reform traditional patties into healthier meat products, adding value to this wild fruit.
Acknowledgements
To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for granting a scholarship (302408/2022-3).
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