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Article

Use of Mucilage from Opuntia ficus-indica in the Manufacture of Probiotic Cream Cheese

by
Pamela Dutra Rodrigues
1,
Isabela de Andrade Arruda Fernandes
2,
Annecler Rech de Marins
3,
Andresa Carla Feihrmann
1,3 and
Raquel Guttierres Gomes
1,*
1
Programa de Pós-Graduação em Engenharia de Alimentos, Universidade Estadual de Maringá (UEM), Maringá 87020-900, PR, Brazil
2
Programa de Pós-Graduação em Engenharia de Alimentos (PPGEAL), Universidade Federal do Paraná (UFPR), Curitiba 81531-980, PR, Brazil
3
Programa de Pós-Graduação em Ciências de Alimentos, Universidade Estadual de Maringá (UEM), Maringá 87020-900, PR, Brazil
*
Author to whom correspondence should be addressed.
Processes 2024, 12(10), 2289; https://doi.org/10.3390/pr12102289
Submission received: 4 September 2024 / Revised: 9 October 2024 / Accepted: 14 October 2024 / Published: 18 October 2024
(This article belongs to the Section Food Process Engineering)

Abstract

:
Cream cheese is a type of fresh cheese with a thin consistency with great potential for adding probiotics. However, artificial thickeners have been used in its production, decreasing consumer satisfaction. This study suggests natural mucilage, specifically from the Cactaceae Opuntia ficus-indica, as a replacement for artificial thickeners due to its thick gelatinous properties. This study evaluated different cream cheese formulations by adding varying concentrations of Opuntia ficus-indica mucilage and the probiotic Lactobacillus acidophilus (L. acidophilus). Four formulations were created: formulation C (control, without mucilage), F1 (containing 1 mL/kg mucilage), F2 (2 mL/kg), and F3 (3 mL/kg mucilage). The physicochemical characteristics (pH, 4.90–5.57; 0.15–0.20% acidity; 1.78–2.42% protein; 29.98–30.88% fat; 38.27–41.63% moisture; and 1.25–1.63% ash) and microbiological analysis met the quality standards required by Brazilian legislation, and the cream cheese showed probiotic potential, with L. acidophilus counts above 108 CFU/mL within four weeks of storage. Regarding sensory evaluation, the texture received one of the highest scores (7.89), followed by aroma (7.11). Therefore, the Cactaceae mucilage has proven to be a viable alternative to replace artificial thickeners in cream cheese, making it an excellent option for probiotic supplementation.

1. Introduction

The global cheese production is showing significant growth in fresh and cream cheese consumption. Global production is estimated to reach 25.2 million tons by 2026, a 0.9% increase compared to 23.9 million tons in 2021 [1]. This growth is attributed to the population and income increase and the fast-food market expansion [2]. Companies have expanded their varieties to meet different applications, such as better spreadability and low-fat content. Furthermore, they also extend to non-dairy products in response to current trends towards vegan products and for people with intolerances and allergies [3].
Cheese is a great way to add probiotic microorganisms, which can improve product quality and consumer health. The relatively high-fat content of cheese helps protect the probiotic microorganisms in the stomach, making it an essential part of many dairy marketing strategies [4]. Fresh cheeses, such as cream cheese, cottage cheese, quark, cottage cheese, and ricotta, can be consumed immediately after production, have a short shelf life, and do not need to mature for a long time. Thus, these products can maintain probiotic viability during storage, making them a better choice for commercially producing probiotic cheeses [2].
Cream cheese, with its slightly buttery and acidic flavor, offers a versatile canvas for various applications in the food industry and for direct consumption. Its creamy texture, ranging from crumbly to spreadable, and shiny appearance make it suitable for incorporating flavors, fibers, herbs, spices, prebiotics, and probiotics. This versatility is intriguing and inspiring for food scientists and industry professionals.
Cream cheese is a dairy emulsion formed by lipids, milk, and water; acidified by lactic acid bacteria; and classified as double-cream cheese with at least (9.0–11.0%) fat content and single-cream cheese with (4.5–5.0%) fat content [2,4]. Cream cheese is made through various manufacturing processes, including homogenization, pasteurization, acidification, coagulation, and whey separation [3]. Salt and stabilizers are added to the curd with homogenization and packaging of the processed product [5].
The texture and sensory qualities of cream cheese have made the product popular for use in bread and bagel toppings, in salad dressing, as an ingredient in recipes, and as a butter substitute [1,6]. In dairy products, thickening, stabilizing, and/or gelling agents such as polysaccharides or hydrocolloids, also known as mucilage, can be added. Mucilage can strengthen the casein network, providing stability and preventing the release of serum from the gel matrix because it is a thickening and stabilizing agent [7,8]. In addition, mucilage exhibits high elastic properties, like synthetic high-elastic polymers such as polyisobutylene. It also exhibits slower responses to deformation when compared to guar and xanthan gums, altering the texture properties of some products [9,10,11].
Artificial food additives are associated with health problems such as allergies and carcinogenicity [12]. Thus, replacing them with safe and stable plant-based compounds may be an exciting approach [13]. The cactus Opuntia ficus-indica is a natural hydrocolloid with excellent physicochemical properties that can be used in the food industry. Its potential for enhancing food quality is a promising avenue for further research and development.
Opuntia ficus-indica is a species of the Cactaceae family native to Mesoamerica. It is a plant with numerous beneficial properties, serving as a source of dietary fiber, vitamins, and many other bioactive compounds with anti-inflammatory, hypoglycemic, and antimicrobial properties [14,15,16]. Different parts of its structure have a mucilaginous mass [17,18], which is composed of heteropolysaccharides, such as uronic acid [10,15,19], and varying proportions of L-arabinose, D-galactose, L-rhamnose, and D-xylose [20]. This cactus is rich in dietary fiber (44.11–49.55%); inorganic elements such as calcium (4780.31–5041.47 mg/100 g) and potassium (4899.25–6612.95 mg/100 g); and phenolic acids (4.1–5.3 g/kg) and flavonoids (3.80–4.85 g/kg), including kaempferol-3-O-rutinoside and isorhamnetin-3-O-rutinoside. In addition, it is a source of carbohydrates, such as glucose (9.30–12.00 g/100 g) and galacturonic acid (6.16–7.90 g/100 g), and it is low in fat (0.76–2.46%) [21]. Therefore, it has a high potential to be considered a functional food.
Changes in consumer demands have shown a great interest in foods that promote health maintenance and prevention of chronic diseases such as liver cancer, hepatic encephalopathy, and inflammatory bowel disease, among others [22,23]. Foods fermented with probiotics can help regulate the intestinal microbiota; improve the permeability and barrier function of the intestine; and produce short-chain fatty acids (SCFAs), which have anti-inflammatory effects. These probiotics also support immune function and can positively impact neurological disorders associated with intestinal dysbiosis [24]. Numerous benefits are attributed to their intake, such as improved gastrointestinal transit, normalization of microbial balance, and competitive exclusion of pathogens [25]. Probiotic dairy products promote health by containing live bacteria, such as lactic acid bacteria (LAB). These bacteria contribute to intestinal balance and strengthen the immune system. In addition to live bacteria, probiotics also produce compounds with health benefits. These include organic acids, exopolysaccharides, bacteriocins, vitamins, peptides, and amino acids [26].
The present study is critical given the scarcity of studies on adding Opuntia ficus-indica mucilage to foods. It aims to produce cream cheese by adding different concentrations of Opuntia ficus-indica mucilage and the probiotic microorganism Lactobacillus acidophilus. This research could open new avenues in functional food production.

2. Materials and Methods

2.1. Extraction of Mucilage from the Opuntia ficus-indica Palm

Opuntia ficus-indica was harvested on the campus of the State University of Maringá, Paraná, Brazil. The mucilage was extracted using a conventional method described in Reference [27], with minor adjustments. To reduce the microbial content, the fruits were cleaned with distilled water and a 1% sodium hypochlorite commercial solution. The fruit was then peeled, diced, and homogenized with 100 mL of distilled water. The mixture was then filtered through cotton cloth, and the filtrate was centrifuged in a refrigerated centrifuge Rotina 380R (Nova Analítica, São Paulo, Brazil) at 6000 RPM, at 10 °C, for 30 min. The supernatant was discarded, and the mucilage was stored at 10 °C.

2.2. Manufacture of Cream Cheese

Four cream cheese formulations were made: formulation C, corresponding to the control sample (without the addition of mucilage); and F1, F2, and F3, with the addition of 1, 2, and 3 mL/kg of Opuntia ficus-indicia palm mucilage, respectively. The amount of mucilage was defined after a preliminary test described by Halmi [28] in a toxicological study of Opuntia ficus-indicia palm mucilage for human consumption.
To manufacture cream cheese, whole milk was pasteurized at 71 °C for 15 s and then cooled to 31 °C. Then, 8.8 mL of coagulant (HA-LA®, Chr. Hansen, São Paulo, Brazil), 7% homofermentative mesophilic culture Lactococcus lactis subsp. lactis and Lactococcus lactis subsp. cremoris (R-704®, Chr. Hansen, São Paulo, Brazil), and 7% probiotic culture containing Lactobacillus acidophilus (LA-5®, Chr. Hansen, São Paulo, Brazil) were added. The mixture was incubated at 27 °C for fermentation until reaching pH 4.6. Subsequently, the mixture was stored at 8 °C for 24 h for whey separation and curd formation. Then, 0.75% sodium chloride and mucilage were added to the curd at different concentrations (F1, F2, and F3) to produce cream cheese. The processed products were stored at 8 °C.

2.3. Physicochemical Characterization

The physicochemical characterization of the mucilage was performed on the day of extraction for the pH, acidity, protein, ash, moisture, and °Brix, according to the official methods of AOAC [29]. The physicochemical characterization of the cream cheese was performed in triplicate, according to the official methods of AOAC [29]. The pH was determined in a digital potentiometer, and titratable acidity was determined by acid–alkalimetric titration, using phenolphthalein as an indicator, on days 1, 7, 14, 21, and 28 of storage. The determination of protein, fat, and ash contents was performed on day one of storage.

2.4. Instrumental Measurements

2.4.1. Colorimetric Analysis

The color measurements were performed using a Minolta® CR10, (Ramsey, NJ, USA), portable colorimeter, with an integration sphere and viewing angle of 3°, with illumination d/3 and illuminant D65, using the CIE L* a* b* system [30]. All determinations were performed in triplicate for four weeks. The hue angle (H°) of the samples was calculated at 7 and 14 days of storage using Equation (1):
H ° = a r c t a n g b * a *

2.4.2. Texture Profile Analysis

The texture profile analysis was performed in triplicate in a texture analyzer (StableTa—TX, Surrey, UK) after 14 days of cream cheese manufacture. The probe P36R was used, and the determinations were performed at 20 °C (Texture Exponet Lite® software version 6.1.4). The test conditions were a pre-test speed of 2.0 mm/s, a test speed of 1.00 mm/s, a post-test speed of 1.00 mm/s, a compression distance of 10 mm, and a contact force of 3.0 g. The hardness (firmness), adhesiveness, cohesiveness, gumminess, springiness, and chewiness were determined. The texture profile parameters were calculated from the force–deformation curves: hardness (N), the force required to reach a given deformation, precisely the maximum force; cohesiveness (dimensionless), the ratio between the area of positive force during the second and the first compression, excluding the decompression area of each cycle; gumminess (N), a simulation of the energy required to disintegrate a semi-solid food into a constant state, calculated as hardness multiplied by cohesiveness; elasticity (cm), the ratio of the distance the samples need to recover after the first compression; and chewiness (N·cm), calculated as hardness multiplied by cohesivity and elasticity [31].

2.4.3. Enumeration of Probiotic Microorganisms

The culture medium MRS Agar specific for Lactobacillus acidophilus (LA-5®, Chr. Hansen, São Paulo, Brazil) was used with depth inoculation for the enumeration of probiotic bacteria. The plates were incubated/inverted in anaerobic jars containing an Anaerobac generator, at 37 °C for 72 h [32]. The analyses were performed in triplicate on days 1, 7, 14, 21, and 28 of storage.

2.4.4. Microbial Control

Total and fecal coliforms were analyzed using the most probable number (MPN) method [33]. The tubes presenting microbial development (turbidity) with or without gas production in the Durhan tubes were observed under a 3-to-6 W UV lamp and 365 nm in a dark booth. The blue fluorescence is a confirmatory test for the presence of E. coli. For molds and yeasts, the surface plating method was used on potato dextrose agar (PDA) acidified with 10% tartaric acid and incubated at 25 °C for 5 days [34]. The analyses were performed in triplicate on days 14 and 28 of storage.

2.5. Gastrointestinal Digestion In Vitro

The simulation of gastrointestinal digestion in vitro was performed according to Correa et al. [35] using artificial saliva, enzyme α-amylase, gastric solution, and artificial intestinal fluid. The final suspension from the intestinal phase was subjected to an analysis of bacterial viability. The results were expressed in colony-forming units per gram (CFU/g).

2.6. Sensory Evaluation

The Human Research Ethics Committee of the State University of Maringá (UEM, Brazil) approved this study under protocol number 27178619.7.0000.0104. In the sensory evaluation, two samples of cream cheese were used according to the processing procedures described in the section on the manufacture of cream cheese: the control sample (without adding mucilage) and the other sample with the addition of 3 mL/kg of Opuntia ficus-indica mucilage. The cream cheese made with the highest concentration of mucilage was selected for the sensory evaluation due to its better uniformity.
The sensory tests were conducted on the first day of product production. One hundred ten participants were recruited from the State University of Maringa (UEM, Brazil) based on their availability, interest in the product, and frequency of consumption. The acceptance test used a nine-point structured hedonic scale, ranging from “liked extremely” to “disliked extremely”, to evaluate the attributes of appearance, aroma, flavor, texture, and overall impression [36]. Additionally, a purchase-intention test was conducted using a 5-point scale with the participants.
The tests were performed in booths with adequate lighting and controlled temperature under white light. The cream cheese was served in disposable plastic cups containing about 25 g of product, coded with three random numbers, accompanied by water and salt cookies. The participants were instructed to consume the cream cheese alone and eat the cookie only to evaluate product spreadability. Drinking water was provided to the participants to cleanse the palate.

2.7. Statistical Analysis

The experiments were performed in triplicate, and the data were analyzed by analysis of variance (ANOVA) and Tukey’s test, using the software R, version 1.2.5019, with a significance level of 5%. The results were expressed as mean values and standard deviation.

3. Results and Discussion

3.1. Physicochemical Characterization of Mucilage

The mucilage obtained from the cladodes of the Opuntia ficus-indica cactus has a pH of 4.75, which is similar to the pH reported by Procacci et al. [37] (4.50), and lower than the pH values of 7.65 (unirrigated plant) and 7.81 (irrigated plant) [38]. It is known from the literature that the pH and ionic strength can impact rheological properties, especially in the presence of Ca2+ and Mg2+ ions rather than Na+ or K+ ions, resulting in higher viscosity at alkaline pH levels [39]. The acidity level, measured at 1.51, aligns with the literature value of 1.40 g·L−1 [37] of tartaric acid equivalent. Additionally, the °Brix value in this study is 0.51, which is higher than the 0.25% reported in [38].
The moisture content obtained was 4.01%, which is close to the values of 4.07 and 4.66 [38] and lower than 8.33% [40]. Moisture is an important factor to measure in mucilage because it is a parameter linked to the quality of the product. Variations in moisture can affect physical properties such as viscosity and texture, as well as physicochemical properties such as water retention capacity and solubility. These properties are fundamental when using mucilage as thickeners, emulsifiers, or stabilizers [41].
The protein content of the studied was 6.70%, which is close to 6.52% [42], and both are higher than Toit et al. [43] (2.7–3.2%). Among the functional properties, the protein content is a highlighted factor due to the interactions of proteins with specific hydrophilic functional groups of polysaccharides, which can affect film formation, emulsification and stabilization capacity, and foam-forming property [37].
The ash content of the mucilage extracted from the cactus Cereus peruvianus was 4.03%, which is higher than the 0.35% ash content of the mucilage of the cladode Opuntia dillenii [44]. High ash values for mucilage extracted from cactus may be related to the high salinity of the soil and mineral bioavailability.
The mucilage obtained from cactus can vary in terms of yield, chemical composition, and physicochemical properties, depending on factors such as the collection site, irrigation, growing conditions, genetic type, age of the plant, and different extraction methods. When the plants are not irrigated, the ash content is lower, and the protein, fiber, carbohydrate, and sugar contents are higher, resulting in greater viscosity and higher quality mucilage [38,45].

3.2. Physicochemical Characterization of Cream Cheese

The physicochemical characterization of the cream cheese is presented in Table 1. The protein content ranged from 1.78 to 2.42%, with no significant differences between the samples, and was lower than the content found in commercial cream cheese (5.7 to 11.1 g) [46]. Cream cheese contains casein and whey proteins in varying proportions, which can form a network that includes fat globules acting as emulsifying agents. The low protein content compared to commercial cream cheese may be due to the formulations’ good gel formation, the raw material’s origin, the whey removal time, and the addition of mucilage [47]. Therefore, the addition of Opuntia ficus-indica mucilage may have contributed to the variation in the protein contents.
No significant differences were observed for the samples’ fat contents; thus, adding mucilage did not interfere with this parameter. Ningtyas et al. [48] reported fat contents for cream cheese between 0.50 and 25.17%, and their values were lower than the values found in the present study. However, it is worth noting that low fat content and high humidity are consistent with less structured products and are more accessible to spread [49]. These changes affect the texture attributes of cream cheese, making it more challenging and impacting consumers’ acceptance of the product [49]. Cheeses with a fat content of ~33% (w/w) are softer and the most marketed [4]. Thus, Codex Alimentarius standards [50] have established the identity standards of whole-fat cream cheese of at least 25% and maximum moisture content of 67%.
Therefore, both fat (29.98–30.88%) and the moisture contents of the cream cheese formulations (38.27 to 41.63%), with no significant difference, were within the levels established by the Codex Alimentarius and the Normative Instruction 71 of 24 July 2020 [51], which establishes the same fat content of the Codex (25 g/100 g of dry extract) and moisture content of up to 78% (78 g/100 g). The moisture content is a crucial factor that significantly influences the texture of a product. A high moisture content means that a substantial amount of water is present, resulting in minimal aggregation of fat and protein particles [7]. High moisture content leads to a softer and less cohesive texture. Therefore, it is essential to manage the moisture content in cream cheese to achieve the desired consistency and structural properties and ensure proper interaction between fat and protein within the matrix [52].
The mucilage extracted from the Opuntia ficus-indica cactus retains more water than other thickeners due to the high concentration of high-molecular-weight polysaccharides, such as arabinose, galactose, xylose, and galacturonic acid. These polysaccharides can form three-dimensional networks in aqueous solutions, increasing their ability to absorb and retain water more efficiently [53]. Additionally, the polysaccharides in Opuntia mucilage have a high viscosity, which contributes to the formation of stable gels [54]. Opuntia mucilage forms a denser and more cohesive network compared to other thickeners, such as xanthan gum or pectin. This results in better water retention due to the interaction between the water molecules and the polysaccharides. It prevents phase separation, such as syneresis in dairy products, and helps maintain the structure and texture of the product [55].
Perveen, Alabdulkarim, and Arzoo [56] studied the effect of temperature on the shelf life, physicochemical parameters, and microbiological characteristics of cream cheese and reported that the samples tended to lose moisture during storage. However, moisture loss was not observed in this study, possibly due to the action of the mucilage used, which contributed to no change in the moisture content of the samples during the 30 days of storage, maintaining the tenderness of the product, which is one of its main characteristics.
The samples’ ash contents (1.25 to 1.63%) were close to the values presented by Silva [57], who studied commercial cream cheeses and found ash contents from 1.10 to 2.39%. The variability in ash content is related to the composition of the milk, which is influenced by the season of the year and the animal’s diet, leading to a decrease or increase in the amount of fat rich in minerals such as potassium, sodium, calcium, magnesium, chloride, and phosphate [58]. The protein composition of milk can also be associated with the ash content since the retention of fat and ash can be favored during the protein coagulation process [59].
The pH values of the formulations (5.10 and 5.48) were slightly higher than those ranging between 4.62 and 5.01 [7]. In the shelf-life study (Figure 1a), the pH values ranged from 5.10 to 5.48 on day one and gradually decreased to the range from 4.97 to 5.32 during storage. According to Ziarno et al. [60], the decrease in pH is related to the consumption of lactose and the production of lactic acid and galactose, showing the metabolic activity of lactic acid bacteria during refrigerated storage. The metabolic activity of probiotic cultures leads to a pH reduction. The metabolic activity of probiotic cultures leads to a decrease in the pH of the cheese. This change influences various biochemical reactions that affect the sensory and structural characteristics of the cheese. As the pH decreases, it can alter the structure of the cheese, impacting its texture and flavor. This process is linked to the production of compounds that can modify the cheese matrix, ultimately contributing to the development of new sensory characteristics [61].
The acidity values were 0.15% for all cream cheese formulations, which ranged from 0.15 to 0.20% over the period studied (Figure 1b). Probiotic microorganisms are known to produce compounds that reduce acidity and contribute to the development of more complex and pleasant flavors. The acidity is important because the production of organic acids and other volatile compounds during the metabolism of probiotics can enrich the sensory profile of cheese, making it more attractive to consumers [62]. Traditional cream cheese is characterized by having a slightly acidic taste [48], and a titratable acidity of up to 0.8% (w/w) is considered necessary to develop an adequate cream cheese flavor [49]. However, acidity is a critical parameter that should be carefully controlled, as it can lead to calcium loss from the protein network and changes in consistency, texture, and flavor, negatively impacting the processed cheeses’ shelf life [63].

3.3. Color Parameters

Table 2 shows the color parameters (L*, a*, and b*) of cream cheese samples and the hue angle (H°) of treatments C, F1, F2, and F3 on days 7 and 14 of storage.
There was no significant difference (p > 0.05) between the color measurements of the four formulations (C, F1, F2, and F3). The L* value represents luminosity, ranging from 0 (black) to 100 (white). A value in the range from 90.15 to 90.91 indicates high luminosity, meaning a product with a very light color that has not been affected by adding cactus-derived mucilage. The L* values ranged from 90 to 91, close to that observed by Lučan et al. [6], who reported an L* value of 97, indicating the white color of the product. No differences were observed between the formulations and the color changes during the 15 days, indicating that the addition of mucilage did not affect the color of the samples.
The a* parameter indicates the intensity of the color from red (+) to green (−), with the initial negative value shifting towards green. After 7 days, the reaction changed it to a positive value. The b* parameter represents a color variation from yellow (+) to blue (−), where a positive value (17.90 to 18.34) indicates a color tending towards yellow. The hue parameter indicates the dominant shade of color, with values around 90° corresponding to shades close to yellow. The change in the a* parameter from negative to positive influenced the change in the tone of the product (hue), possibly due to the addition of cactus mucilage.

3.4. Microbiological Characterization

The probiotic strain Lactobacillus acidophilus’s count ranged from 107 to 109 CFU/g during the 30-day storage period. Across different formulations and throughout the study, there was a consistent decrease in the population of the probiotic microorganism (refer to Table 3). Ningtyas, Bhandari, Bansal, and Prakash [64] reported the viability of cream cheese with Lactobacillus rhamnosus (encapsulated and non-encapsulated), with counts above 106 CFU/g. Speranza et al. [65] studied functional cream cheese with Bifidobacterium animalis subsp. lactis (DSM 10140) or Lactobacillus reuteri (DSM 20016) and prebiotics and reported probiotic bacteria counts above 109 CFU/g during the 28 days of storage. Tologana et al. [61] examined the impact of single and mixed cultures on the survival of probiotics in cream cheese during shelf life. Therefore, the formulations of the present study have the probiotic potential for food supplementation. With the addition of Opuntia ficus-indica mucilage, cream cheese can be consumed in small daily portions as an alternative to performing probiotic effects with health benefits due to its functional properties.
When controlling the microbiological quality of dairy products, it is necessary to comply with the tolerance limit for total and fecal coliforms, molds, and yeasts to guarantee hygienic production conditions without risking consumers’ health [66]. Coliforms are considered indicator microorganisms; their presence in certain foods indicates exposure to conditions that can lead to contamination by pathogenic organisms. Coliform counts indicate bad hygienic practices; that is, the conditions of treatment and handling of food represent a potential danger [66,67,68]. In the present study, the enumeration of total coliforms, fecal coliforms, molds, and yeasts throughout the storage was within hygienic and sanitary standards (Table 4). Lemes et al. [69] also reported satisfactory sanitary conditions, with counts for molds and yeasts (3.6 × 103 CFU/g) higher than the present study (1 × 101 to 1 × 102) CFU/g, with lower total and fecal coliforms counts (0.3 MPN/g). The international microbiological criteria for dairy products have established that cheese made with heat-treated milk must have a maximum coliform content of 5 MPN/g [70]. Thus, the cream cheese with the addition of mucilage was within the microbiological standards that infer product quality.

3.5. Gastrointestinal Digestion In Vitro

The results of L. acidophilus viability at 28 days of storage after digestion in vitro are shown in Figure 2, with a significant difference between probiotics (p < 0.05). A decrease in L. acidophilus counts was observed after passage through the gastrointestinal tract, with values between 0.07 and 0.97 log·g−1 when compared to cream cheese before digestion. These results confirm that cream cheese, with the addition of Opuntia ficus-indica mucilage, can be a matrix for probiotic bacteria.
Studies have shown that L. acidophilus is sensitive to gastric acid and pepsin, presenting lower counts, as reported by Nejati et al. [71]. Schillinger et al. [72] conducted a study on six strains of L. acidophilus and verified that the number of microorganisms in the gastrointestinal-tract simulation increased.
The fat in dairy products helps create a denser and more protective matrix for probiotic microorganisms. This is because fat and total solids have a buffering effect, which aids in the survival of probiotics [73]. In addition, the effect of adequate storage at low temperatures also affects the survival of the probiotics [74] and the optimal-growth pH, which ranges from 5.5 to 6.0 for L. acidophilus [75].
In the present study, even after reducing probiotic counts, the products presented viable counts higher than the level (>106 CFU/g) necessary to demonstrate health benefits. Factors such as the type of processing used, compounds present or added to the product, pH value, and storage influence the viability of probiotic bacteria [76].

3.6. Texture Profile Analysis

Texture profile analysis is used for the quality control of a commercial product based on more straightforward and more reproducible instrumental techniques [46]. Cream cheese has a more compact and creamy texture characteristic, responsible for the product’s softness [4]. The texture of cream cheese can be affected by several factors, including the physicochemical composition (moisture, protein, fat, and hydrocolloids) and processing conditions, such as pH, temperature, and homogenization process [48]. Table 5 shows the results of the parameters firmness, hardness, springiness, cohesiveness, and gumminess.
An increase in the concentration of mucilage decreased the firmness and hardness of the cream cheese. It is important to note that the moisture content plays a significant role in determining the firmness and hardness of cheese. High moisture content weakens the casein network, leading to a softer texture in cream cheeses. Therefore, adding gums can help retain moisture within the cheese, resulting in a softer texture [77,78].
This behavior was observed in the present study, in which the decrease in firmness and hardness was inversely proportional to the increase in moisture contents.
Cohesiveness measures the extent to which the sample can be deformed before it breaks and is inversely proportional to fat and moisture contents. Lower fat and moisture contents provide a high casein content, which contributes to the protein–protein interactions (gelation), which leads to the protein matrix’s hardening, consequently providing the product with a more cohesive characteristic [63]. This study observed higher cohesiveness for the control sample, which contained lower moisture and protein contents (0.46). In contrast, the other formulations showed cohesiveness between 0.39 and 0.45, values lower than those reported by Lemes et al. [69], who produced cream cheese with enzymatic milk coagulation and added Bacillus sp. P45 and reported cohesiveness between 0.70 and 0.82. According to the authors, high cohesiveness characteristics can favor the development of a more elastic gel, which requires more force to deform the cream cheese.
Springiness is related to the speed and extent of recovery from a compression force [48]. In the present study, there was no significant difference between the samples for the parameter springiness, which ranged from 0.82 to 0.96. Shanhraki et al. [76] conducted a study on adding natural herbal gums, Lepidium perfoliatum, and linseed seeds to cream cheese. They monitored the texture profile for 45 days and found that the results were consistently better throughout the study period than adding cactus mucilage.
Regarding the gumminess attribute, they observed a decrease in gumminess as the mucilage concentration increased (from 933.04 to 608.87 g). This means that the process required lower force with increased mucilage concentration, producing more excellent softness. Portaghi et al. [79] described that incorporating gums decreased the attribute gumminess, and similar results were reported by Milani et al. [80].
The nanomechanical analysis considers the nanometric scale, including resistance, elasticity, and structure. Acidification lowers the pH, destabilizing the casein micelles. When the pH is close to 4.6 (the isoelectric point of casein), the proteins aggregate and form a gel network. This protein coagulation results in a cohesive gel that retains water and fat, contributing to the cream cheese’s creamy and smooth texture [81]. Acidification can alter the elasticity and cohesiveness by changing the way proteins form stable bonds. Emulsifiers are added to maintain this characteristic texture and prevent the separation of water and fat, ensuring uniform consistency for longer. Acidification is crucial for the formation of the characteristic creaminess and smoothness in cream cheese [82]. A study [7] on structure formation in processed cheese demonstrated that various factors affect the viscosity profile, including the formation of the casein matrix and interaction with fat globule surfaces for emulsification. While protein–fat interactions are essential in structuring, protein–protein interactions are also significant. Atomic force microscopy (AFM) has been instrumental in characterizing casein’s microstructural and mechanical properties to understand its structure better.

3.7. Sensory Evaluation

As shown in Table 6, no significant differences were observed for the attributes appearance, aroma, flavor, overall impression, and purchase intention among the samples, except for the attribute texture, which showed a significant difference between the control and the sample with the addition of 3 mL/kg of mucilage. The average scores were 7.09 and 8.67 for the control and sample F3, respectively. Thus, adding mucilage led to a higher score on the hedonic scale equivalent to “liked moderately”.
For the attribute appearance, the values ranged from 7.55 to 7.85, corresponding to the term “liked moderately”, with no significant differences. Cream cheese is still widespread in Brazil for daily consumption, and this fact may have affected this result.
No significant differences were observed for the aroma and flavor of the sample with the addition of mucilage compared to the control. Therefore, adding mucilage from plants had no negative impact on the acceptability of cream cheese, which usually has a characteristic aroma and flavor.
Our global print scores (7.52 to 7.67) were higher compared to the results of Correia’s [70] study, which studied cream cheese with raw or extruded (SF) sorghum flours with brown pericarp and tannins (7.00 a 7.65). Therefore, adding mucilage and probiotics had no negative impact on the cream cheese’s appearance, aroma, flavor, overall impression, and purchase intention. Similarly, Speranza et al. [65] evaluated the supplementation of cream cheese by adding prebiotics and the probiotics Bifidobacterium animalis subsp. Lactis (DSM 10140) and Lactobacillus reuteri (DSM 20016) and also found no negative effect of probiotic bacteria on the sensory acceptance of this functional product.

4. Conclusions

The mucilage from Opuntia ficus-indica proved to be an excellent substitute for artificial hydrocolloids in cream cheese, maintaining its identity standards and positively influencing the texture of the food, both concerning the analytical standards and consumers’ acceptance. In addition, cream cheese presented the viability of the probiotic microorganism in simulated gastrointestinal conditions, adding value to the product and possibly bringing health benefits to the consumer. For future research, it would be valuable to investigate the rheological properties of the mucilage, as well as its physicochemical composition and functionality.

Author Contributions

Formal analysis, P.D.R., I.d.A.A.F. and A.R.d.M.; Resources, R.G.G.; Writing—review & editing, A.C.F. and R.G.G.; Supervision, R.G.G.; Project administration, R.G.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and COMCAP/UEM.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. pH (a) and acidity (b) of cream cheese.
Figure 1. pH (a) and acidity (b) of cream cheese.
Processes 12 02289 g001
Figure 2. Gastrointestinal digestion in vitro for cream cheese.
Figure 2. Gastrointestinal digestion in vitro for cream cheese.
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Table 1. Physicochemical characterization of cream cheese with the addition of Opuntia ficus-indica mucilage.
Table 1. Physicochemical characterization of cream cheese with the addition of Opuntia ficus-indica mucilage.
Time (Days)Formulations 1
CF1F2F3
Protein (%)12.16 ± 0.26 a2.42 ± 0.83 a1.78 ± 0.34 a2.35 ± 0.81 a
Lipids (%)129.98 ± 0.22 a30.01 ± 0.06 a30.59 ± 0.02 a30.88 ± 0.04 a
Moisture (%)138.88 ± 0.15 a38.27 ± 0.54 a39.16 ± 0.03 a39.88 ± 0.10 a
1439.17 ± 0.37 a39.21 ± 0.15 a39.33 ± 0.24 a39.51 ± 0.15 a
2838.96 ± 0.40 a41.63 ± 0.27 a40.07 ± 0.41 a39.98 ± 0.29 a
Ash (%)11.63 ± 0.22 a1.62 ± 0.24 a1.50 ± 0.07 a1.25 ± 0.02 a
pH15.48 ± 0.01 a5.10 ± 0.01 a5.25 ± 0.03 a5.25 ± 0.04 a
Acidity10.15 ± 0.01 a0.15 ± 0.01 a0.15 ± 0.01 a0.15 ± 0.01 a
a Mean values with different letters show significant differences between treatments (p < 0.05) according to Tukey’s test. 1 Formulations: C (without the addition of mucilage), F1 (1 mL/kg of mucilage), F2 (2 mL/kg of mucilage), and F3 (3 mL/kg of mucilage).
Table 2. Instrumental color of cream cheese with the addition of Opuntia ficus-indica mucilage.
Table 2. Instrumental color of cream cheese with the addition of Opuntia ficus-indica mucilage.
Time (Days)Formulations 1
CF1F2F3
L*790.97 ± 0.34 a90.39 ± 0.22 a90.64 ± 0.59 a91.15 ± 0.31 a
1490.15 ± 0.20 a90.59 ± 0.10 a90.57 ± 0.52 a90.91 ± 0.31 a
a*7−0.52 ± 0.03 a−0.54 ± 0.02 a−0.54 ± 0.06 a−0.53 ± 0.08 a
140.11 ± 0.03 a0.09 ± 0.02 a0.08 ± 0.04 a0.09 ± 0.05 a
b*718.02 ± 0.01 a18.28 ± 0.17 a17.94 ± 0.36 a18.23 ± 0.15 a
1418.34 ± 0.03 a17.90 ± 0.11 a18.09 ± 0.17 a18.24 ± 0.16 a
7−88.34 a−88.58 a−88.27 a−89.12 a
1489.65 b89.71 b89.74 b89.71 b
a–b Mean values with different letters show significant differences between treatments (p < 0.05) according to Tukey’s test. 1 Formulations: C (without the addition of mucilage), F1 (1 mL/kg of mucilage), F2 (2 mL/kg of mucilage), and F3 (3 mL/kg of mucilage).
Table 3. Counts of the probiotic Lactobacillus acidophilus.
Table 3. Counts of the probiotic Lactobacillus acidophilus.
DaysCounts of the Probiotic Lactobacillus acidophilus (CFU/g)
CF1F2F3
18.19 × 108 ± 0.04 aA7.87 × 107 ± 0.07 bA8.00 × 107 ± 0.01 bA9.20 × 109 ± 0.01 aA
77.05 × 108 ± 0.01 aA7.44 × 107 ± 0.04 bA7.20 × 107 ± 0.08 bB9.01 × 108 ± 0.10 aA
148.00 × 107 ± 0.04 bB6.55 × 107 ± 0.12 cB7.80 × 107 ± 0.01 bB8.98 × 108 ± 0.07 aA
217.18 × 107 ± 0.02 aB4.59 × 107 ± 0.01 bC6.98 × 107 ± 0.02 aB7.94 × 107 ± 0.03 aB
288.03 × 107 ± 0.02 aB4.19 × 107 ± 0.01 cC3.23 × 107 ± 0.02 cC6.95 × 107 ± 0.02 bB
Mean ± standard deviation. Results with different letters in the same row are significantly different according to Tukey’s test (p ≤ 0.05). Results with capital letters in the same column are significantly different according to Tukey’s test (p ≤ 0.05). Formulations: C (without the addition of mucilage), F1 (1 mL/kg of mucilage), F2 (2 mL/kg of mucilage), and F3 (3 mL/kg of mucilage).
Table 4. Microbiological characterization of cream cheese.
Table 4. Microbiological characterization of cream cheese.
MicroorganismsTime (Days)Formulations 1
CF1F2F3
Total coliforms
(MPN 2/g)
14
28
1
1
1
2
1
2
3
2
Fecal coliforms
(MPN/g)
14
28
-
<2
-
-
<1
<2
<2
<2
Molds and yeasts
(CFU 3/g)
14
28
<1 × 101
<1 × 101
<1 × 101
<1 × 101
<1 × 101
<1 × 102
<1 × 101
<1 × 102
1 Formulations: C (without the addition of mucilage), F1 (1 mL/kg of mucilage), F2 (2 mL/kg of mucilage), and F3 (3 mL/kg of mucilage). 2 MPN: most probable number. 3 CFU: colony-forming units.
Table 5. Texture profile analysis of cream cheese with the addition of Opuntia ficus-indica mucilage.
Table 5. Texture profile analysis of cream cheese with the addition of Opuntia ficus-indica mucilage.
Formulations 1
CF1F2F3
Firmness (g)1819.21 ± 459.29 a1722.73 ± 197.69 a1485.33 ± 960.93 a1357.86 ± 123.14 a
Hardness (g)2151.94 ± 874.97 a2071.71 ± 575.36 a1945.16 ± 671.83 a1354.15 ± 34.76 a
Cohesiveness0.46 ± 0.11 a0.45 ± 0.03 a0.41 ± 0.08 a0.39 ± 0.04 a
Springiness (m)0.82 ± 0.17 a0.87 ± 0.20 a0.96 ± 0.03 a0.87 ± 0.03 a
Gumminess (g)933.04 ± 170.06 a826.73 ± 181.50 a766.56 ± 267.00 a608.87 ± 39.33 a
a Mean values with different letters show significant differences between treatments (p < 0.05) according to Tukey’s test. 1 Formulations: C (without the addition of mucilage), F1 (1 mL/kg of mucilage), F2 (2 mL/kg of mucilage), and F3 (3 mL/kg of mucilage).
Table 6. Sensory evaluation of cream cheese with the addition of Opuntia ficus-indica mucilage.
Table 6. Sensory evaluation of cream cheese with the addition of Opuntia ficus-indica mucilage.
Samples 1EMD 2
CF3
Appearance7.85 a7.55 a0.34
Aroma7.07 a7.11 a0.40
Flavor7.55 a7.37 a0.40
Texture7.09 a8.67 b0.33
Overall impression7.67 a7.52 a0.31
Purchase intention1.97 a2.19 a0.25
a–b Mean values with different letters show significant differences between treatments (p < 0.05) according to Tukey’s test. 1 Formulations: C (without the addition of mucilage) and F3 (3 mL/kg of mucilage). 2 EMD: expected minimum difference.
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MDPI and ACS Style

Rodrigues, P.D.; Fernandes, I.d.A.A.; de Marins, A.R.; Feihrmann, A.C.; Gomes, R.G. Use of Mucilage from Opuntia ficus-indica in the Manufacture of Probiotic Cream Cheese. Processes 2024, 12, 2289. https://doi.org/10.3390/pr12102289

AMA Style

Rodrigues PD, Fernandes IdAA, de Marins AR, Feihrmann AC, Gomes RG. Use of Mucilage from Opuntia ficus-indica in the Manufacture of Probiotic Cream Cheese. Processes. 2024; 12(10):2289. https://doi.org/10.3390/pr12102289

Chicago/Turabian Style

Rodrigues, Pamela Dutra, Isabela de Andrade Arruda Fernandes, Annecler Rech de Marins, Andresa Carla Feihrmann, and Raquel Guttierres Gomes. 2024. "Use of Mucilage from Opuntia ficus-indica in the Manufacture of Probiotic Cream Cheese" Processes 12, no. 10: 2289. https://doi.org/10.3390/pr12102289

APA Style

Rodrigues, P. D., Fernandes, I. d. A. A., de Marins, A. R., Feihrmann, A. C., & Gomes, R. G. (2024). Use of Mucilage from Opuntia ficus-indica in the Manufacture of Probiotic Cream Cheese. Processes, 12(10), 2289. https://doi.org/10.3390/pr12102289

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