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Article

Innovative Fermented Beverages Based on Bread Waste—Fermentation Parameters and Antibacterial Properties

by
Krzysztof Juś
1,
Mateusz Ścigaj
2,
Daniela Gwiazdowska
1,*,
Katarzyna Marchwińska
1 and
Wiktoria Studenna
2
1
Department of Natural Science and Quality Assurance, Institute of Quality Science, Poznań University of Economics and Business, Al. Niepodległości 10, 61-875 Poznań, Poland
2
Scientific Student Association “Inventum”, Department of Natural Science and Quality Assurance, Institute of Quality Science, Poznań University of Economics and Business, Al. Niepodległości 10, 61-875 Poznań, Poland
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(12), 5036; https://0-doi-org.brum.beds.ac.uk/10.3390/app14125036
Submission received: 15 April 2024 / Revised: 20 May 2024 / Accepted: 4 June 2024 / Published: 10 June 2024
(This article belongs to the Special Issue Functional Bakery Products: Technological, Chemical and Nutritional Modification)
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Abstract

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In response to the contemporary and future challenges for the food production sector in achieving sustainable development goals, this work presents an innovative solution for the management of problematic food waste, such as bakery waste. Prepared beverages based on unused wheat–rye bread fermented using lactic acid bacteria, may be a good starting point for the further development of an innovative, functional food product. Moreover, fermented drinks based on waste from the bakery industry are consistent with the assumptions of sustainable production, and the results obtained in this work may provide interesting information for the circular economy and waste management development.

Abstract

Faced with challenges related to environmental degradation and the growing need for sustainable development, the food sector must look for innovative and ecological production solutions. One of the increasingly popular directions is the zero-waste approach, which limits waste generation and enables its reuse. This research aimed to evaluate selected quality indicators of the lactic acid fermentation process of beverages based on waste from the bakery industry (wheat–rye bread) to determine the optimal fermentation conditions using two strains of lactic acid bacteria: Lacticasibacillus paracasei and Lactiplantibacillus plantarum. Preliminary process optimization was carried out, taking into account the beverage composition, fermentation time, and starting culture. The process evaluation and the selection of the optimal variant were based on the microbiological quality, pH value, and antimicrobial activity of fermented beverages. The results showed that the bread waste may constitute a base for obtaining fermented beverages as evidenced by the high number of lactic acid bacteria, above 108 CFU/mL, and low pH values (≤3.5) after the appropriate incubation time. Fermented beverages exhibited antibacterial properties against tested indicator microorganisms, which confirmed their functional properties. The analysis of the obtained results and the adopted assumptions enabled the selection of the most optimal variant—the beverage with ground flaxseed, fermented by L. paracasei for 24 h. The conducted research indicates great potential for lactic acid fermentation in the management of bakery waste to create innovative, sustainable food products with probiotic potential.

1. Introduction

Food waste is a global problem, causing significant economic losses around the world and negatively affecting the environment [1]. The problem is deepened by the fact that the world population may reach approximately 10 billion in 2050, resulting in a growing demand for various types of products, especially food [2]. It is estimated that food production, including agricultural production, will increase from approximately 47% to 102% during this time to meet the growing demand for food [3]. However, it should be taken into account that the intensification of food production largely contributes to the degradation of the natural environment. The negative effects of food production include, among others, excessive greenhouse gas emission, associated with increasingly frequent weather anomalies, loss of biodiversity, bioaccumulation of toxic substances, reduction in forest area, and depletion of natural resources [4,5]. Consumerism also contributes to the intensification of production, which, regardless of social, climatic, or ecological costs, leads to overproduction and generates excessive waste amounts. It is estimated that approximately one-third of food produced is wasted annually on a global scale, which results in social costs (including waste of resources) and negatively affects the financial results of producers [6]. Food waste losses may occur at various stages of the food supply chain, from primary production, including agriculture and animal production, through processing, packaging, and distribution processes, to losses caused by the consumer [7]. Food loss and waste generation depend on the type of food, with greater loss and waste occurring in perishable foods such as fruit and vegetables. However, bakery waste is also a serious global problem.
Bread is one of the most important products consumed around the world, and its global production reaches >100 million tons per year. Therefore, it is a commonly wasted food in most developed countries, which is a particularly serious problem in Europe [8]. It is difficult to determine the exact amount of wasted bread, as the use of water and energy in the production and transport process should also be taken into account; however, it is estimated that 10% of all bread produced is wasted worldwide [9]. For example, in the United Kingdom (UK), bread is the second most frequently wasted food. It is estimated that every day in UK homes, the equivalent of 25 million slices of bread or 1,300,000 loaves is thrown away [10]. In Poland, research carried out by the Federation of Polish Food Banks in 2012–2018 indicates that bread is the most frequently thrown-away product, and the percentage of respondents declaring waste of bread ranged from 49 to 62% in this period [11].
Therefore, various ways of using bakery waste are being undertaken towards valorization into value-added products considering that bread contains a wide range of nutrients. In 100 g of bread, there are approximately 50–70 g of carbohydrates, 8–10 g of protein, 1–5 g of fat, and trace amounts of phosphorus [12]. Bread waste can be used as biomass for the production of biohydrogen, regarded as clean and renewable energy [13], as well as for the production of ethanol, considered one of the most promising fuel sources [14,15]. Dubrovskis and Plume [16] described biogas production from damaged bread. Moreover, bread waste can be used as feed for livestock [17,18] as well as a substrate for hydroxymethylfurfural synthesis and for the production of pigments, proteins, or aroma compounds [19,20,21]. Many researchers emphasize that bakery waste usage should largely focus on processing it into new food products. This is possible to achieve by using the fermentation processes with various microorganisms. Lactic acid fermentation is considered a safe and practical way to acidify food products and extend their shelf life because the metabolites produced and the low pH inhibit the growth of undesirable microorganisms. The nutritional, health-promoting, and sensory values of fermented products are also important. The increase in nutritional value is related, among others, mainly to the production of amino acids and different bioactive compounds [22,23]. The health benefits associated with consuming fermented foods and beverages include increased digestibility, antimicrobial [24], antihypertensive, antioxidant [25], and even immunostimulating [26] properties. Some lactic acid bacteria (LAB) strains also produce exopolysaccharides (EPS), which increase the viscosity of the fermented product [27,28]. An example of using lactic acid fermentation to reuse bread waste is research conducted by Immonen et al. [29]. The authors assessed the potential of two LAB strains (Weissella confusa A16 and Pediococcus claussenii E-032355T) to transform bakery waste into an EPS-enriched bread slurry dedicated as an ingredient in the production of baked goods.
It is worth emphasizing that fermented products are considered functional foods, which constitutes a valuable part of the food market, especially in highly developed countries. A constant development and increase in the value of this branch of the food industry is expected around the world [30]. There are many definitions of functional food in the literature, but generally this product category includes unmodified (natural) food as well as food in which ingredients have been modified (including those increasing their bioavailability), added or removed using cultivation conditions or technological/biotechnological processes, which make it possible to obtain specific health-promoting effects or improve general well-being after consumption [31]. Beverages are one of the most popular products in the functional food category mainly due to the convenience of consumption as well as easier distribution and storage [32]. A wide range of traditional, non-dairy fermented drinks are produced around the world [33]. Examples of such products are Boza made from wheat, rye, millet, maize, and other cereals, known in Bulgaria, Albania, Turkey, and Romania [34], Bushera from sorghum consumed in Uganda [35], or Togwa prepared by fermentation of maize flour in Africa [36]. In the case of fermented beverages with potential probiotic properties, it is important to maintain the cell count at an appropriate level throughout the shelf life of the product [37] as well as during the passage through the digestive system [38]. One of the basic procedures aimed at increasing the survival of LAB in a product is the addition of various types of products/substances with prebiotic effects [39]. An interesting example is ground flaxseed, which, in addition to its high content of dietary fiber (prebiotic effect), is also a valuable source of substances such as α-linolenic acid, omega-3 acid, proteins, and lignan, making it an ingredient with functional potential [40]. The literature contains research results showing the positive effect of ground flaxseed on the stability of LAB in various types of products. For example, Vesterlund et al. [41] (2012) found a positive effect of adding ground flaxseed to the matrix on the increased viability of Lacticaseibacillus rhamnosus GG during storage for a period of 14 months. A positive effect of flaxseed on LAB survival was also reported by HadiNezhad et al. [42] (2013), who found a significantly higher number of LAB in kefir with the addition of flaxseed muciligate after 28 days of storage at 4 °C compared to unfortified kefir. In turn, Bialasová et al. [43] (2018) reported a higher number of Lactobacillus acidophilus CCDM 151 in milk with the addition of ground flaxseed (by 0.8 log CFU/mL) after 16 h of fermentation compared to milk without the addition of flaxseed.
Despite studies confirming the positive impact of LAB fermentation on food waste reuse, it should be emphasized that products obtained through spontaneous fermentation are not repeatable and may differ in composition and sensory characteristics. Standardization of the process requires specific starter cultures. However, this involves selecting the appropriate strain with specific properties. Therefore the present study aimed to design innovative beverages produced by lactic acid fermentation of waste from the bakery industry and to evaluate selected quality characteristics of the beverages for the initial selection of optimal fermentation conditions. Appropriately selected LAB strains and the addition of ground flaxseed to increase the nutritional value of bakery waste for bacteria were used in the fermentation process.

2. Materials and Methods

2.1. Chemicals, Materials, and Microorganisms

2.1.1. Chemicals

Microbiological media used for the studies were obtained from BioMaxima (Poland) and included as follows: de Man, Rogosa, and Sharpe (MRS) broth and MRS LAB-AGAR™, nutrient broth, Sabouraud dextrose with chloramphenicol LAB-AGAR™, Mueller-Hinton broth, trypticasein soy broth (TSB), and TBX LAB-AGAR™. Chemical reagents such as glucose (Stanlab, Lublin, Poland), sodium chloride (POCh, Gliwice, Poland), and pH buffers (Sigma-Aldrich, Steinheim, Germany), used for the tests were of analytical grade.

2.1.2. Research Material

Wheat–rye crushed stale bread was the base for the preparation of fermented beverages. Research material was stored in sealed bags in a dry location at room temperature (±20 °C). Ground flaxseed (LenVitol®, Oleofarm, Wrocław, Poland) was purchased from a local pharmacy in Poland.

2.1.3. Microorganisms

Bread-waste beverages (BWBs) were fermented using two strains of lactic acid bacteria as starter cultures: Lactiplantibacillus plantarum DKK 003 and Lacticaseibacillus paracasei DKK 002. Both strains were from the collection of the Department of Natural Science and Quality Assurance, Poznań University of Economics and Business. The starter microorganisms were cultured before each use on MRS liquid medium at 30 °C for 24 h, and long-term storage was maintained in cryoprobes on MRS broth with 80% glycerol (in a 1:1 ratio) at −22 °C.
The antimicrobial properties of the fermented BWBs were tested against four indicator bacteria, namely Staphylococcus saprophyticus ATCC 49453, Micrococcus luteus ATCC 4698, Escherichia coli ATCC 25922, and Pseudomonas fluorescens ATCC 13525 from the American Type Culture Collection (ATCC). Tested bacteria were freshly cultured before the experiments on nutrient broth or trypticasein soy broth (for M. luteus) for 24 h at a temperature of 30 or 37 °C (depending on the strain), according to ATCC data. Indicator strains were stored long-term at −22 °C using Microbank® cryogenic beads (BioMaxima, Lublin, Poland).

2.2. Methods

2.2.1. Bread-Waste Beverage Fermentation

BWBs were prepared using 10 g of wheat–rye crushed stale bread with or without 5 g of ground flaxseed, depending on the variant. Next, 200 mL of boiling water was added and samples were left for 24 h to soften the ingredients. An amount of 5 g of glucose was added to all samples, which were then inoculated with 1 mL of LAB cultures per 100 mL. Two strains were used to inoculate the beverages: L. plantarum and L. paracasei, as well as a mixture of both strains (1:1, v:v); the density of the inoculum was 1010 CFU/mL. Finally, the inoculated beverages were incubated at 30 °C for 6, 8, 12, 24, and 48 h. After fermentation, the liquid phase was poured off from the solid phase (pulp), and the obtained beverage was used for testing. The selection of the optimal BWB variant involved the selection of strains and fermentation time, as well as chosen quality characteristics: microbiological quality, pH value, and antimicrobial activity (Figure 1).

2.2.2. Determination of Microbiological Quality of Fermented BWBs

The microbiological quality of the prepared fermented BWB samples was determined by the standard plate method. The tested samples were placed in sterile blender bags (BagFilter S, Interscience, Saint Nom, France) and mixed with sterile saline solution (in ratio 10:90, v:v) and homogenized in a stomacher (BagMixer 400 W, Interscience, Saint Nom, France) for 5 min. The tests were performed included determining the total number of LAB on MRS agar (30 °C for 48 h), the total number of fungi (yeast and molds) on Sabouraud agar with chloramphenicol (25 °C for 5 days), and the presence of E. coli bacteria on TBX agar (37 °C for 24 h). The results are presented as average values from three parallel repetitions.

2.2.3. Measurement of the pH of Fermented BWBs

The pH value of the fermented BWBs was measured using an Orion Star A111 pH meter from Thermo Scientific, Waltham, MA, USA. The glass electrode was placed in the well-stirred test sample and the result was read after the readings stabilized. The measurement was carried out in three repetitions at room temperature (22.0 ± 2.0 °C).

2.2.4. Antimicrobial Properties of Fermented BWBs

The antimicrobial activity of the prepared fermented BWBs was determined using the microdilution method on 96-well microtiter plates according to the methodology described by Kaczmarek et al. [44] with some modifications. Samples of fermented BWBs were centrifuged twice at 10,000 rpm/min for 10 min using a Centrifuge 5804R. Next, a series of two-fold dilutions was prepared on 96-well microplates in MH broth medium (for S. saprophyticus, E. coli, and P. fluorescens) and TSB (for M. luteus) at a ratio of 80:80 µL. Fresh, 24 h cultures of indicator microorganisms were then used to prepare suspensions in broth mediums with a final density of 0.5 McFarland which corresponds 105 CFU/mL. The prepared plates were incubated for 24 h at 30 or 37 °C, depending on the indicator microorganism. After incubation, the optical density of the prepared cultures was measured at 600 nm using a BioTek EPOCH2 Microplate Reader (Agilent, Santa Clara, CA, USA). The antimicrobial activity of the BWBs was tested in the concentration range of 6.25–50%. The results are expressed as the average (from three parallel repetitions) percentage of inhibited growth of indicator microorganisms calculated based on the formula described by Marchwińska et al. [45]:
A % = 1 − X _ O D B − X _ O D C X _ O D I − X _ O D M × 100 %
where A% is the antibacterial properties of the tested BWBs, X _ O D B is the mean optical density of bacterial culture with the addition of fermented BWBs, X _ O D C is the mean optical density of the culture medium with the addition of fermented bread beverage, X _ O D I is the mean optical density of bacterial inoculate (without fermented BWB), and X _ O D M is the average optical density of the pure medium.
The minimal inhibitory concentration (MIC) was determined next based on the previously calculated antibacterial activity of the fermented BWBs, assuming that the inhibition of the indicator microorganisms’ growth had to be no less than 90%.

2.2.5. Statistical Analysis

The results of the studies are presented as the arithmetic mean (±standard deviation) from three parallel replicates. The results obtained from the microbiological quality and pH value determination were subjected to one-way analysis of variance (ANOVA) using Tukey’s test with a significance level of p < 0.05. Microsoft Excel® (Microsoft 365 MSO) and IBM SPSS Statistics 28 (PS IMAGO PRO 8.0) programs were used for statistical analyses.

3. Results

3.1. Microbiological Quality and pH of BWBs

In the first part of the experiment, the suitability of the L. plantarum and L. paracasei strains as starter cultures for the fermentation of bread waste was assessed. Microbiological quality including the number of LAB, the number of fungi, and the presence of E. coli as well as the pH value were monitored at specific intervals during 48 h fermentation as the basic quality parameters chosen to evaluate the process (Table 1). It was crucial to determine the minimal fermentation time in which the LAB population would reach at least 108 CFU/mL so that the beverage could provide health-promoting properties and inhibit the development of undesirable microorganisms.
The obtained results showed that the expected level of bacterial counts—108 log CFU/mL—was achieved in most of the prepared fermented beverages after 8 h of fermentation, except for the beverage with the addition of ground flaxseed inoculated with a mixture of LAB cultures, where the LAB concentration was 7.50 log CFU/mL. It is worth emphasizing that in some variants, including BWBs with L. plantarum and L. paracasei as well as BWBs with flaxseed inoculated with L. paracasei, the level of 108 log CFU/mL was reached after 6 h. The highest number of LAB (at the level of 109 CFU/mL) was obtained after 24 h of fermentation in beverages fermented with L. paracasei with and without the addition of ground flaxseed as well as after 48 h in beverages with the addition of flaxseed inoculated with L. plantarum, for which the results were 9.24, 9.53, and 9.63 log CFU/mL, respectively. It should be underlined that only the result for the BWB with flaxseed fermented by L. plantarum after 48 h was significantly different from all obtained results. It is also worth noting that the BWBs inoculated with the LAB mixture achieved lower numbers, with the highest result of 8.95 in the BWB after 24 h and 8.93 in the BWB with flaxseed after 48 h of fermentation. No presence of E. coli or fungi (both yeast and filamentous fungi) was detected in all prepared BWBs variants.
During fermentation, as the number of bacteria increased, a significant decrease in the pH value of all beverages was observed. No significant differences in pH values were observed only in the case of BWBs fermented with LAB mixture (between 6 and 8 h of fermentation) as well as BWBs with and without flaxseed inoculated with L. plantarum (between 8 and 12 h of fermentation). The lowest pH values were recorded in BWBs fermented by L. paracasei and LAB mixture after 48 h of fermentation, with pH of 2.77 and 2.81, respectively. The beverages with the addition of ground flaxseed inoculated with L. paracasei and LAB mixture after 48 h of fermentation were also characterized by pH values < 3.0; however, these values were significantly higher compared to BWBs without the addition of flaxseed. It is worth noting that the addition of ground flaxseed increased the pH value of the beverages regardless of the inoculant (pH values were significantly higher at each hour of fermentation compared to samples without ground flaxseed). Lower pH values were observed in beverages fermented by L. paracasei (with and without the addition of ground flaxseed) and the mixture compared to the L. plantarum strain.

3.2. Antimicrobial Properties of BWBs

3.2.1. Minimal Inhibitory Concentration Determination

One of the parameters characterizing fermented beverages is antimicrobial activity, with the determining minimum inhibitory concentration (MIC) of the indicator microorganisms’ growth (Table 2). The results indicate that the main factor determining the MIC values was fermentation time. It was found that the determination of the MIC value of BWBs in the tested concentration range (from 6.25 to 50%) was possible as the fermentation process was extended. For most BWB variants, the MIC against E. coli, S. saprophyticus, and P. fluorescens was >50% (from 6 to 12 h of fermentation) and 25 or 50% (BWBs after 24 and/or 48 h fermentation). The exception was the BWB variant with the addition of ground flaxseed fermented with L. paracasei, where MIC against P. fluorescens was determined at 12.5% concentration after 48 h fermentation. The lowest MIC value was determined for M. luteus, indicating the highest sensitivity of this microorganism. The MIC value in the tested range of BWB concentrations was determined for BWBs after 6 h of fermentation (25 to 50%), while after 24 and 48 h the MIC value for all prepared variants of fermented drinks was 6.25%.

3.2.2. Effect of Fermented BWBs on Bacterial Growth Inhibition

The antimicrobial activity of BWBs was considered an added value of prepared products and was examined against both gram-positive and gram-negative bacteria (Figure 2, Figure 3 and Figure 4). Since the exact MIC value was not determined for many samples, indicating that it was higher than the highest concentration of the beverage used, antibacterial activity is presented as the degree of inhibition of the growth of indicator microorganisms by the tested concentrations. This also enables the observation of activity changes during the fermentation process.
The strongest antibacterial effect of fermented BWBs inoculated with L. plantarum (Figure 2) was recorded for beverages with the addition of ground flaxseed at 50% concentration, which inhibited bacterial growth of all tested microorganisms at a level exceeding 70% starting from 6 h of fermentation. The exception was S. saprophyticus, whose growth was inhibited at this level by BWBs from 8 h of fermentation. The greatest sensitivity to BWBs inoculated with L. plantarum, both without and with the addition of flaxseed, was demonstrated by M. luteus, the growth of which was inhibited by 90 to 100% at BWB concentrations of 25 and 50% from 6 h of fermentation. A strong antagonistic effect was also observed against E. coli, inhibited by BWBs after 6 h fermentation at levels of 43 and 41% (BWBs without flaxseed) and 82 and 65% (BWBs with flaxseed) at 25 and 50% concentrations, respectively. P. fluorescens showed similar sensitivity; however, strong inhibition of bacterial growth was observed with BWBs at a 50% concentration. A longer fermentation time increased the antibacterial activity of BWBs against both gram-negative bacteria, with higher activity demonstrated by beverages with ground flaxseed. The least sensitivity to BWBs with L. plantarum was demonstrated by S. saprophyticus, the growth of which was inhibited to a significant extent (>90%) only after BWBs fermented for 24 h (BWB without flaxseed) and after 12 h of fermentation (BWB with flaxseed) mainly at 50% concentration.
In Figure 3, antimicrobial activity of BWBs inoculated with L. paracasei is presented. Similarly to beverages with L. plantarum, the highest antibacterial activity towards all tested indicator bacteria was demonstrated by BWBs fermented for 24 and 48 h. BWBs without ground flaxseed inhibited the growth of E. coli, P. fluorescens, and S. saprophyticus at a significant level (>80%) at 50% concentrations after 24 and 48 h fermentation. In comparison, at 25% concentration, high growth inhibition (89%) was observed only against P. fluorescens by BWBs fermented for 48 h. In turn, BWBs with the addition of ground flaxseed demonstrated higher antimicrobial activity than those without. The significant inhibition of the growth of microorganisms was observed at a 50% concentration (above 60% of growth inhibition) after 6 h fermentation (towards E. coli and S. saprophyticus) and after 8 h fermentation (towards P. fluorescens). Concerning P. fluorescens, the effect of the drink increased significantly after 8 h fermentation, while after 48 h, a high (>90%) inhibition of bacterial growth was found by the lower concentration of the beverages—12.5%. The most sensitive microorganism to the effects of drinks fermented with L. paracasei (both without and with the addition of flaxseed) was M. luteus, for which growth inhibition in a wide range of beverage concentrations (6.25–50%) was observed after 6 h of fermentation.
The BWBs fermented with the LAB mixture had similar antimicrobial activity to beverages fermented with single LAB cultures; however, the spectrum of activity at individual concentrations and incubation times was noticeably lower (Figure 4). Only in relation to M. luteus, BWBs fermented with the LAB mixture exhibited a strong inhibitory effect (in the range of 60–100%) after just 6 h fermentation in the entire range of tested concentrations (6.25–50%). The addition of ground flaxseed increased antimicrobial activity, but this relationship was observed mainly at 50% BWB concentration (against P. fluorescens and S. saprophyticus) and 50 and 25% concentrations (against E. coli). BWBs without the addition of ground flaxseed showed a strong antibacterial effect (above 90% growth inhibition) against E. coli and S. saprophyticus after 48 h of fermentation (at 50% concentration), while against P. fluorescens, such a high level of growth inhibition was obtained both after 24 and 48 h fermentation at 50% beverage concentration.

3.3. Selection of the Optimal BWB Variant

The assessment of the BWB fermentation process based on chosen quality features enabled the selection of a beverage variant that would constitute the basis for further development of the innovative product. The selection process included several steps, which are presented in Figure 5.
First, the success of the fermentation process and microbiological quality were assessed based on LAB amount and pH value. In most BWB variants, the LAB amount reached the satisfactory level of 108 CFU/mL after 8 h of fermentation. The LAB number will determine, among others, the shelf life and health benefits of the product, so this value should be as high as possible. Therefore, the best variants are BWB with flaxseed fermented with L. plantarum for 48 h and BWBs without and with flaxseed fermented by L. paracasei for 24 h, in which the LAB count reached 109 cfu/mL. Statistical analysis confirmed the significantly higher LAB amount in these variants, although the LAB number in BWB with flaxseed fermented by L. paracasei for 24 h and BWB without flaxseed fermented with the LAB mixture for 24 h did not differ significantly.
The second quality criterion chosen to evaluate the prepared BWBs was the pH value. The appreciable acidity of the beverages indicates that the fermentation process is proceeding correctly and positively affects the microbiological safety and stability of the final product. Therefore, the study assumed that the optimally prepared fermented BWBs should have a pH of ≤3.5. Obtaining the desired degree of acidity depended on the fermentation time. In most variants, a pH level below 3.5 was achieved after 24 h, except for BWB with flaxseed fermented by L. plantarum, where a pH of 3.37 was achieved after 48 h fermentation. The lowest pH values (<3.0) were obtained for BWBs without and with the addition of flaxseed, fermented by L. paracasei and the LAB mixture after 48 h of fermentation. Interestingly, the highest LAB population was not recorded in the BWB variants with the lowest pH. For example, in the BWB with flaxseed fermented by L. plantarum for 48 h (the highest LAB number), the pH value (3.37) did not differ significantly from BWBs with flaxseed fermented by L. paracasei (3.21) and BWBs fermented with LAB mixture (3.01 and 3.23 with and without flaxseed, respectively) for 24 h, for which LAB amount was significantly lower.
The LAB number and pH were used together as the third criterion, emphasizing the economic aspect of the process. As BWBs fermented for both 24 and 48 h had good and comparable quality parameters, it can be assumed that it will be more profitable from a production point of view to carry out fermentation in a shorter time, reducing the production costs. Taking into account these parameters, the optimal variants were BWBs without and with the addition of ground flaxseed, fermented with L. paracasei and a LAB mixture for 24 h.
The last parameter for selecting the optimal BWB variant was its antimicrobial activity. The results confirmed that to obtain the best functional properties (in the context of antibacterial properties), it is necessary to carry out fermentation for at least 24 h. After this fermentation time, it was possible to determine the MIC values for most variants, and a broader spectrum of the activity of the beverages against indicator microorganisms was observed. Additionally, the conducted research indicated that the ground flaxseed addition resulted in increased antagonistic activity of the fermented BWBs. These observations indicated that adding a nutrient-rich ingredient could increase the product’s functional properties.
Taking into account the antibacterial properties of the fermented BWBs, as well as the previous premises, the optimal variant was the BWB with the addition of flaxseed fermented with L. paracasei for 24 h. For this variant, it was possible to determine the MIC against all indicator microorganisms, and for P. fluorescens this value was the lowest (MIC = 25%) compared to the other variants. Since these types of products are most often consumed without dilution (100% concentration), the criterion for selecting other variants for further development may be the LAB number and pH value. The stronger antibacterial effect of fermented BWBs with flaxseed indicates that these variants meet the product functional criterion to a greater extent. BWBs with flaxseed fermented by LAB mixture are also worth considering, as multi-strain fermented products may be more acceptable by consumers.

4. Discussion

In response to contemporary and future challenges for the food production sector in achieving sustainable development goals, the work presents an innovative solution for managing problematic food waste, such as bakery waste. It is also in line with current trends concerning the development of non-dairy fermented products including fermented beverages, which is associated with the increase in various health problems such as lactose intolerance.
Applying lactic acid fermentation to cereal raw materials may be problematic due to the fact that LAB does not have good properties in converting starch into lactic acid, although some strains, including L. plantarum, show such activity [46]. However, the beneficial properties of LAB make them an attractive subject of research for new fermented products. It is worth emphasizing that bakery waste is rarely used as a matrix for composing a fermented beverage, so literature data in this area are strongly limited.
Zamfir et al. [47] used wheat bran, a major by-product of wheat processing, containing different nutritional constituents, such as proteins, carbohydrates, vitamins, and minerals, together with red beetroot/carrots to prepare fermented beverages. As the starter culture, two strains of L. plantarum (BR9 and P3) and L. acidophilus IBB801 were used. Similar to the results obtained in our work, in the final product the pH was, in most cases, below 3.5 and spoilage microbiota such as enterobacteria were not detected. Sigüenza-Andrés et al. [48] described beverages based on flour from bread waste fermented using commercial starters Nu-trish® LGG® and Nu-trish® BY-01 DA. Regarding the number of LAB and Bifidobacterium in beverages after 24 h of fermentation, the authors recorded values similar to the present study. Beverages fermented with Nu-trish® LGG® starter reached bacterial levels above 108 CFU/g, while beverages fermented with the Nu-trish® BY-01 DA saturator acquired lower values of 103–107 CFU/g, depending on the prepared variant. Moreover, Sigüenza-Andrés et al. [48] found that the content of organic acids in the tested beverages ensures the pH value of the beverages, allowing the microbiological stability of the product to be maintained. Lactic acid fermentation of bread slurries using the L. rhamnosus GG ATCC 53103 strain was also carried out by Nguyen et al. [49]. In the prepared fermented bread slurries (2.5% w/w, dry weight) after 16 h of fermentation, the authors recorded L. rhamnosus at a concentration of 7.7 log CFU/g and a pH close to 3.5. The authors obtained a higher number of L. rhamnosus, above 108 CFU/g, with an increased share of bread slurry (to 5% w/w, dry weight) after 16 and 24 h of fermentation. While the pH value of the fermented bread slurries prepared by Nguyen et al. [49] was close to the pH of the BWBs tested in this study (after 24 h fermentation), the LAB number obtained by Nguyen et al. [49] was lower.
Determining the antimicrobial activity of the fermented beverages was crucial due to their potential health-promoting properties; however, the presented data also indicate that the activity of fermented BWBs depended mostly on the genus of indicator bacteria, as well as on the concentration of the beverages. The higher degree of growth inhibition of indicator microorganisms was also observed with the extension of the fermentation time. In most cases, the addition of ground flaxseed to beverages had a positive effect on increasing the antimicrobial activity of BWBs.
The antibacterial properties of fermented drinks are rarely an evaluation criterion. Very few data apply to products made from waste. Typically, antimicrobial properties are determined for strains subsequently used to produce the beverages. Nevertheless, some authors have also evaluated these properties. Similar to our results, Zamfir et al. [47] observed inhibition of Listeria monocytogenes, Salmonella enterica, Staphylococcus aureus, and E. coli by fermented beverages made from wheat bran and root vegetables. Singh et al. [50] reported the antimicrobial activities of whey-based fermented soy beverages with the addition of curcumin. The product obtained by fermentation with L. acidophilus NCDC 195 (LA195) and Streptococcus thermophilus NCDC323 (ST323) demonstrated activity towards E. coli, B. cereus, S. aureus, L. monocytogenes, Shigella dysenteriae, and Salmonella typhi. The authors observed that with the increasing storage time, the antibacterial activity decreased. Undhad et al. [51] studied the antimicrobial activity of fermented soy-based beverages towards some pathogenic strains and found higher antimicrobial activity against gram-positive bacteria (S. aureus, B. cereus, and L. monocytogenes) than against gram-negative pathogens (E. coli, S. typhi, and S. dysenteriae). The antimicrobial properties of fermented beverages can be explained by the presence of metabolites produced by LAB, such as organic acids or bacteriocines, although some components of the raw materials as well as additives may also affect the activity. Antimicrobial properties were also described for non-dairy beverages fermented by microorganisms other than LAB such as kombucha. Al-Mohammadi et al. [52] observed inhibition of the growth of S. aureus and E. coli, while other authors also reported activity against different species of Candida (C. krusei, C. glabrata, C. albicans, C. tropicalis), Haemophilus influenzae [53], Staphylococcus epidermidis, S. aureus, M. luteus, Salmonella typhimurium, L. monocytogenes, or Pseudomonas aeruginosa [54].
The antimicrobial properties of such products are related to the presence of metabolites such as organic acids, mainly acetic acid and catechins [55]. It should be emphasized that antimicrobial activity constitutes a significant added value not only due to their connection with the potentially probiotic properties of bacteria, but also because they protect against the development of undesirable microorganisms.

5. Conclusions

Current and future challenges facing the food production sector in terms of environmental and social aspects (ensuring food security) encourage producers to look for more sustainable solutions both in the area of production processes and the design of new products. This work attempts to preliminarily optimize the process of lactic acid fermentation of beverages based on waste from the bakery industry. Our research is consistent with current trends related to waste management and sustainable food production. The obtained results indicate that bakery waste (wheat–rye bread) may constitute the basis for obtaining beverages through lactic acid fermentation. Very interesting and important results were obtained in studies on the antimicrobial properties of prepared fermented BWBs, which were significantly influenced by fermentation time, composition, and LAB culture. Extending fermentation time and adding ground flaxseed had a key impact on increasing the antibacterial activity of fermented BWBs. The research has shown that when developing new fermented products, it is important to select the appropriate composition and production conditions to obtain products with the best possible quality parameters. The omission of any of the assessed parameters may lead to the selection of inappropriate process conditions or beverage composition, thus contributing to the deterioration of the quality or functionality of the final product.
Our research is also a good starting point for further work on product development. Prior to the product-testing stage, it is necessary to develop flavor proposals for BWBs as well as determine their microbiological stability during storage to ensure an appropriate level of product safety. The finally developed beverages should also be fully analyzed to determine the content of macro- and microelements, and LAB survival tests should be performed (e.g., metagenomic analysis) to ensure appropriate quality characteristics of BWBs. Additionally, further LAB strains can still be tested in terms of the effectiveness of fermentation of bread waste in order to possibly create a multi-strain beverage that could be an interesting proposition for consumers. Marketing research such as consumer acceptance and preferences and unit packaging design should be considered as interesting and valuable complementary research. Conducting the above-mentioned complementary research would provide the basis for attempting to commercialize the designed innovative beverages based on bread waste.

Author Contributions

Conceptualization, K.J. and M.Ś.; methodology, K.J., M.Ś. and D.G.; validation, K.J., D.G. and K.M.; formal analysis, K.J., M.Ś., D.G., K.M. and W.S.; investigation, K.J., M.Ś., D.G. and W.S.; resources, K.J., D.G. and K.M.; data curation, K.J., M.Ś. and D.G.; writing—original draft preparation, K.J., M.Ś., D.G., K.M. and W.S.; writing—review and editing, K.J., D.G. and K.M.; visualization, K.J., M.Ś. and D.G.; supervision, K.J. and M.Ś.; project administration, K.J. and D.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Polish Ministry of Science and Higher Education (MNiSW) as part of the “Student Scientific Association Create Innovations” program, project number SKN/SP/569408/2023.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 14 05036 g001
Figure 1. Scheme of the bread-waste beverage (BWB) selection procedure.
Figure 1. Scheme of the bread-waste beverage (BWB) selection procedure.
Applsci 14 05036 g001
Applsci 14 05036 g002
Figure 2. Antimicrobial activity of BWBs inoculated with L. plantarum against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
Figure 2. Antimicrobial activity of BWBs inoculated with L. plantarum against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
Applsci 14 05036 g002
Applsci 14 05036 g003aApplsci 14 05036 g003b
Figure 3. Antimicrobial activity of BWBs inoculated with L. paracasei against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
Figure 3. Antimicrobial activity of BWBs inoculated with L. paracasei against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
Applsci 14 05036 g003aApplsci 14 05036 g003b
Applsci 14 05036 g004
Figure 4. Antimicrobial activity of BWBs inoculated with a mixture of LAB strains against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
Figure 4. Antimicrobial activity of BWBs inoculated with a mixture of LAB strains against indicator microorganisms. (A–D)—BWBs without flaxseed; (E–H)—BWBs with flaxseed.
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Applsci 14 05036 g005
Figure 5. Selection of the optimal BWB variant based on the adopted assumptions. BWB: bread waste beverages without flaxseed; BWBF: bread waste beverages with flaxseed; Lp: fermented by L. plantarum; Lpc: fermented by L. paracasei; Mix: fermented by a mixture of LAB; 0–48 h: fermentation time.
Figure 5. Selection of the optimal BWB variant based on the adopted assumptions. BWB: bread waste beverages without flaxseed; BWBF: bread waste beverages with flaxseed; Lp: fermented by L. plantarum; Lpc: fermented by L. paracasei; Mix: fermented by a mixture of LAB; 0–48 h: fermentation time.
Applsci 14 05036 g005
Table 1. Total number of lactic acid bacteria (LAB) and pH values of fermented BWBs.
Table 1. Total number of lactic acid bacteria (LAB) and pH values of fermented BWBs.
Incubation TimeL. plantarumL. paracaseiMIX of LAB
[CFU/mL]pH[CFU/mL]pH[CFU/mL]pH
BWBs without flaxseed
0 h7.41 CDE ± 0.135.21 n ± 0.027.39 CDE ± 0.095.09 m ± 0.016.79 A ± 0.015.02 m ± 0.04
6 h8.23 HIJ ± 0.464.30 hi ± 0.058.06 GH ± 0.034.28 hi ± 0.037.20 CD ± 0.144.23 gh ± 0.01
8 h8.38 IJK ± 0.253.87 f ± 0.028.47 JKL ± 0.013.63 e ± 0.038.11 GHI ± 0.054.13 g ± 0.02
12 h8.51 J–M ± 0.133.66 e ± 0.138.63 K-O ± 0.043.59 e ± 0.018.12 GHI ± 0.013.89 f ± 0.01
24 h8.60 K–O ± 0.013.37 d ± 0.029.53 TU ± 0.033.05 b ± 0.018.95 RS ± 0.073.01 b ± 0.02
48 h8.80 M–R ± 0.013.22 c ± 0.028.75 L-R ± 0.032.77 a ± 0.038.60 K–N ± 0.122.81 a ± 0.05
BWBs with flaxseed
0 h7.39 CDE ± 0.185.29 no ± 0.037.12 BC ± 0.025.30 no ± 0.026.82 AB ± 0.025.34 o ± 0.04
6 h7.84 FG ± 0.014.43 j ± 0.068.41 IJK ± 0.074.80 l ± 0.027.63 EF ± 0.094.99 m ± 0.05
8 h8.26 HIJ ± 0.044.24 gh ± 0.038.24 HIJ ± 0.184.21 gh ± 0.057.50 DE ± 0.034.63 k ± 0.01
12 h8.88 N-R ± 0.033.86 f ± 0.038.87 N–R ± 0.024.15 g ± 0.028.64 K-P ± 0.034.36 ij ± 0.01
24 h8.94 PR ± 0.033.64 e ± 0.029.24 ST ± 0.023.21 c ± 0.018.9 OPR ± 0.033.23 c ± 0.01
48 h9.63 U ± 0.393.37 d ± 0.008.83 N–R ± 0.072.94 b ± 0.018.93 PR ± 0.082.99 b ± 0.01
Averages with different lowercase letters (a–o) are significantly different at p ˂ 0.05 (comparison of pH value of BWBs). Averages with different capital letters (A–U) are significantly different at p ˂ 0.05 (comparison of the LAB amount in BWBs).
Table 2. Minimal inhibitory concentration (%) of fermented BWBs towards indicator microorganisms.
Table 2. Minimal inhibitory concentration (%) of fermented BWBs towards indicator microorganisms.
VariantIncubation TimeBWBs Inoculated with L. plantarum
E. coliP. fluorescensS. saprophyticusM. luteus
BWBs
without flaxseed		6 h>50>50>5025
8 h>50>50>5025
12 h>50>50>5012.5
24 h>5050506.25
48 h5050506.25
BWBs
with flaxseed		6 h>50>50>5025
8 h>50>50>5012.5
12 h5050506.25
24 h5050506.25
48 h2525256.25
BWBs inoculated with L. paracasei
BWBs
without flaxseed		6 h>50>50>5050
8 h>50>50>5050
12 h>50>50>5050
24 h>5050506.25
48 h5050506.25
BWBs
with flaxseed		6 h>50>50>5050
8 h>50>50>5050
12 h>5050>5050
24 h5025506.25
48 h2512,5256.25
BWBs inoculated with MIX of LAB strain
BWBs
without flaxseed		6 h>50>50>5050
8 h>50>50>5050
12 h>50>50>5025
24 h>5050>506.25
48 h5050506.25
BWBs
with flaxseed		6 h>50>50>5050
8 h>50>50>5050
12 h>50>50>5050
24 h5050>506.25
48 h2525506.25
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Juś, K.; Ścigaj, M.; Gwiazdowska, D.; Marchwińska, K.; Studenna, W. Innovative Fermented Beverages Based on Bread Waste—Fermentation Parameters and Antibacterial Properties. Appl. Sci. 2024, 14, 5036. https://0-doi-org.brum.beds.ac.uk/10.3390/app14125036

AMA Style

Juś K, Ścigaj M, Gwiazdowska D, Marchwińska K, Studenna W. Innovative Fermented Beverages Based on Bread Waste—Fermentation Parameters and Antibacterial Properties. Applied Sciences. 2024; 14(12):5036. https://0-doi-org.brum.beds.ac.uk/10.3390/app14125036

Chicago/Turabian Style

Juś, Krzysztof, Mateusz Ścigaj, Daniela Gwiazdowska, Katarzyna Marchwińska, and Wiktoria Studenna. 2024. "Innovative Fermented Beverages Based on Bread Waste—Fermentation Parameters and Antibacterial Properties" Applied Sciences 14, no. 12: 5036. https://0-doi-org.brum.beds.ac.uk/10.3390/app14125036

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