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Article

Alginate/Fish Gelatin-Encapsulated Lactobacillus acidophilus: A Study on Viability and Technological Quality of Bread during Baking and Storage

by
Milad Hadidi
1,*,
Nava Majidiyan
2,
Aniseh Zarei Jelyani
3,
Andrés Moreno
1,
Zahra Hadian
4 and
Amin Mousavi Khanegah
5,*
1
Department of Organic Chemistry, Faculty of Chemical Sciences and Technologies, University of Castilla-La Mancha, 13071 Ciudad Real, Spain
2
Department of Veterinary Medicine, Urmia Branch, Islamic Azad University, Urmia 57169-63896, Iran
3
Food Control Laboratory, Department of Food and Drug, Shiraz University of Medical Science, Shiraz 71348-14336, Iran
4
Department of Food Technology Research, Faculty of Nutrition Sciences and Food Technology, National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran 19395-4741, Iran
5
Department of Food Science and Nutrition, Faculty of Food Engineering, University of Campinas, São Paulo 13083-852, Brazil
*
Authors to whom correspondence should be addressed.
Foods 2021, 10(9), 2215; https://doi.org/10.3390/foods10092215
Submission received: 21 August 2021 / Revised: 11 September 2021 / Accepted: 15 September 2021 / Published: 18 September 2021
(This article belongs to the Section Grain)
Browse Figures
Versions Notes

Abstract

:
In the present study, Lactobacillus acidophilus LA-5 was microencapsulated in sodium alginate, followed by fish gelatin coating (0.5, 1.5, and 3%). The survival of L. acidophilus in bread before and after encapsulation in alginate/fish gelatin during the baking and 7-day storage was investigated. Moreover, the effect of alginate/fish gelatin-encapsulated L. acidophilus on the technological properties of bread (hardness, staling rate, water content, oven spring, specific volume, and internal texture structure) was evaluated. Compared with control (free bacteria), encapsulated L. acidophilus in alginate/fish gelatin showed an increase in the viability of bread until 2.49 and 3.07 log CFU/g during baking and storage, respectively. Good viability of (106 CFU/g) for probiotic in encapsulated L. acidophilus in alginate/fish gelatin (1.5 and 3%, respectively) after 4-day storage was achieved. Fish gelatin as a second-layer carrier of the bacteria had a positive effect on improving the technical quality of bread. Furthermore, the staling rate of bread containing encapsulated L. acidophilus alginate/fish gelatin 0.5, 1.5, and 3% decreased by 19.5, 25.8, and 31.7%, respectively. Overall, the findings suggested encapsulation of L. acidophilus in alginate/fish gelatin capsule had great potential to improve probiotic bacteria’s survival during baking and storage and to serve as an effective bread enhancer.

Graphical Abstract

1. Introduction

Bread is an innovative field in the probiotic food sector and has attracted rising interest in research. Due to the high temperatures during the bread baking process, probiotics in bread are challenging [1]. Probiotics are live bacteria and yeasts promoted as having health benefits to the host when consumed adequately. Moreover, these microbes must survive the processing and storage of food, as the presence of large numbers of unstressed and viable microbial cells at the time of using them is responsible for the health benefits. The probiotic counts between 106 and 109 CFU/g are universally admitted in the food [2,3].
A promising strategy to enhance probiotic bacteria’s survival is to encapsulate probiotic cells in a protective capsule. The viability of probiotics in a solid matrix during heat processes is influenced by the composition of the matrix [4]. Zhang et al. [5] encapsulated Lactobacillus plantarum in four encapsulating materials, including reconstituted skim milk, Arabic gum, maltodextrin, and inulin. They found that the survival of probiotics in bread during baking was significantly influenced by the approach used to incorporate strains and physicochemical properties of coating materials. In a similar study, coated alginate-based microcapsules with an egg stearic acid/albumen matrix were used to encapsulate Lactobacillus acidophilus. The viability of encapsulated bacteria was found higher during the baking of bread [6]. Encapsulation of lactobacilli in alginate beads has been found to enhance their thermal stability and increase survival during heating and storage [7,8]. In this regard, present studies mainly focused on the encapsulation of probiotics and their viability on bread. In contrast, investigations on the impact of encapsulated probiotics in biopolymers such as alginate and fish gelatin on staling and technological quality of bread during storage remain scarce.
Hydrocolloids are an excellent ingredient for improving the technical quality of bread. Among them, one of the best materials for making hydrogels is fish gelatin. Compared to mammalian gelatins, fish gelatin does not induce bovine spongiform encephalopathy and has no religious limitations. Moreover, fish gelatin is microbiologically stable and derived from byproducts and waste from the fisheries and aquaculture industry, thus decreasing environmental pollution and production costs [9]. In addition, fish gelatin improves the cohesivity and stability of the network structure through electrostatic interactions and stable intermolecular hydrogen bonds between the cationic amine group in fish gelatin (-NH3+) and the carboxylate group in alginate (-COO-) [10].
As a complex process, bread staling is a critical quality factor for wheat bread, including moisture loss and textural changes. The bread staling process involves several mechanisms such as migration of moisture, starch–gluten interaction, and retrogradation of starch and amylopectin [11]. Water migration and hardness can also significantly limit bread quality during storage and shelf life of baked products [12].
This investigation aims to create new functional food to improve the viability of L. acidophilus LA-5 during bread baking and storage using microencapsulation in sodium alginate, followed by fish gelatin-coating (0.5, 1.5, and 3%). Moreover, adding alginate/fish gelatin-encapsulated L. acidophilus on the technological qualities of bread such as hardness, staling rate, water content, oven spring, specific volume, and internal texture structure during 7 days of storage was studied.

2. Materials and Methods

2.1. Preparation of Probiotics Bacterial Cell

The Lactobacillus acidophilus (LA-5) probiotic strain was provided by Christian Hansen (Horsholm, Denmark). MRS broth (Neogen Corporation, Lansing, MI, USA) was employed to prepare the probiotic culture as the growth medium. A single microorganism colony was inoculated in the sterile growth medium (10 mL) and pre-cultured at 37 °C for 12 h. Afterward, 1% v/v inoculum of L. acidophilus were sub-cultured in MRS broth (100 mL) at 37 °C without agitation for 24 h. The L. acidophilus cell was harvested and washed with sterile 0.9% saline solution by centrifugation at 4 °C and 10,000× g for 10 min (BXT-H165A, Baxit, China).

2.2. Encapsulation in Alginate/Fish Gelatin Matrix

L. acidophilus was microencapsulated in sodium alginate according to the emulsion method defined by Moghanjougi et al. [13] with minor modifications. Firstly, sodium alginate (2% w/v) and fish gelatin (0.5, 1.5, and 3% w/v) solutions were separately prepared in deionized water and sterilized at 121 °C for 15 min (15 psi). Then, 10 mL of microbial suspension was mixed with 40 mL of sodium alginate solution in a sterile condition, then added steadily by sterile syringe into a sterilized solution containing 198 g of rapeseed oil and 2 g of Tween 80 and mixed using a magnetic stirrer (3500, Anzeser, Tokyo, Japan) at 750 rpm for 20 min. Next, sterilized calcium chloride solution (80 mL, 0.1 M) was added to the mixture by syringe as a dropper, and then the solution was blended on a magnetic stirrer for 10 min at 100 rpm. Sterile peptone water (80 mL) was added for separating the phases, and the emulsion was stabled for 30 min. After the sedimentation of formed beads, the microcapsules were divided by centrifugation at 400× g for 10 min at 4 °C, and the oily fraction was eliminated. The obtained beads were washed twice with sterile physiology serum (0.9%) to remove residuals. Afterward, microcapsules were immersed in 10 mL of fish gelatin solution (0.5, 1.5, and 3% w/v) and blended for 30 min at 500 rpm, transferred into a sterile glass container, and dried in a lyophilizer (RL-50DG, Really, Henan, China) at −56 °C for 24 h. Finally, prepared capsules were kept in a refrigerator.

2.3. Breadmaking

Bread samples were produced according to the following formulation: 200 g of wheat flour, 8 g of sugar, 3 g of salt, 2 g of instant yeast, 6 g of butter, and UHT skim milk (130 g) with probiotics added. Bread with non-encapsulated bacteria addition was prepared as the control. For dough preparation, the dry ingredients were mixed in a stand mixer (Malka-20, Amasadora, Alicante, Spain) at 40 rpm for 1 min, then milk and probiotic were added and kneaded at 80 rpm for 7 min. After 5 min of resting, the dough was divided into balls of 50 g and proofed at 85% RH and 40 °C in a climate chamber (NT-125, Always here, China) for 60 min. Samples were baked at 175 °C for 6 min in an electric oven (Maxima Deluxe 5, Granada, Spain). Finally, bread was packed in polyethylene bags and kept at room temperature and 55% RH for 7 days in the climate chamber.

2.4. Viable Cell Counts of L. acidophilus

Five gram of samples (dough or bread) was aseptically homogenized with sterile peptone water (45 mL, 0.1% w/w) in a stomacher (400, Seward, AK, USA). Serial dilutions of the suspensions (100 μL) were prepared in sterile peptone water (900 μL), and 100 μL solution was plated onto the MRS agar broth (Neogen, Corporation, Lansing, MI, USA) incorporated with 200 mg/L natamycin (Merck Chemical Co., Darmstadt, Germany). Natamycin was used for inhibiting the yeast’s growth on the MRS agar plate, which did not affect the probiotics’ growth [14]. The plates were counted after incubation at 37 °C for 48 h. The results were expressed as log CFU/g.

2.5. Encapsulation Efficiency, Particle Size, and Zeta Potential of Capsules

The particle size and electrical charge of the capsules were measured by a laser diffraction Mastersizer (Malvern Instruments, Worcestershire, UK) and a Zeta seizer (Malvern Ltd., Malvern, UK), respectively [15].
The encapsulation efficiency was estimated as the percentage of loaded cells in the capsule relative to the initial L. acidophilus cells according to the following equation:
Encapsulation efficiency (%) = N/N0 × 100
where N represents the viable count of encapsulated cells after releasement and N0 is a total number of viable free cells added initially to matrix material during the encapsulation process [16].

2.6. Determination of Hardness and Staling Rate

A Brookfield CT3 texture analyzer was employed to determine crumb hardness. A bread slice (thickness of 2.5 cm) was compressed up to 40% deformation with a 38.1 mm acrylic probe at 120 mm/min speed and 1 min of hold time. The hardness is related to the peak force of the first compression cycle. The staling rate of bread samples was estimated as increases in crumb hardness after the final day of storage [11] as follows:
Staling rate = [hardness (day 7 − day 0)/days of storage]

2.7. Determination of Moisture Content

The moisture content of samples was measured according to the Approved Method of AACC 44-15.02 [17]. The samples were dried in an oven at 105 °C for 8 h. Moisture content was estimated for fresh bread and after storage (1, 4, and 7 days) as the following formula:
Moisture content (%) = [initial weight − weight after drying/initial weight] × 100

2.8. Oven Spring and Specific Volume Index

The difference in dough height before and after baking was considered the oven spring of bread [18]. The baked sample was weighed after 30 min cooling (g), and its volume (cm3) was measured according to the rapeseed displacement method. The specific volume (cm3/g) was estimated as bread volume/bread weight [19].

2.9. Internal Texture Structure Analysis

The image scanner studied the bread’s internal texture structure (Sony 70-DM, Tokyo, Japan) and analyzed it using ImageJ analysis software (ver. 2.3). The cropped images (4 × 4 cm2) were converted to 8-bit grayscale binary images with a resolution of 600 dpi to quantify porosity (ratio pore area/16 cm2), cell density (cells/cm2), and cell average area (ratio pore area/number of cells) [11].

2.10. Statistical Analysis

All experimental data were expressed as means ± standard deviations (n = 3) after passing the analysis of variance (ANOVA) and Duncan’s multiple range tests using SPSS statistics software (ver. 22.0). p < 0.05 was accepted to be statistically significant.

3. Results and Discussion

3.1. Encapsulation Efficiency, Particle Size, and Zeta Potential of Capsules

The encapsulation efficiency of L. acidophilus was 92.3% for the alginate as a single carrier, similar to the results observed by Moghanjougi et al. [13] by 95.5% for L. acidophilus and Jouki et al. [16] by 93.1% for Lactobacillus casei in alginate beads. The encapsulation efficiency of L. acidophilus significantly increased along with the increase of concentration of fish gelatin from 92.3 to 98.68% (Table 1). Some factors like the hydrogen bonding between carboxylate groups of fish gelatin and sodium alginate and good interaction between these biopolymers could increase encapsulation efficiency [20,21]. The range of particle size of encapsulated L. acidophilus in alginate/fish gelatin was from 289.8 to 736.5 μm with a relatively narrow range of size distribution. The particle size of encapsulated L. acidophilus in alginate/fish gelatin ranged. The size of capsules is an important physical property that affects the bioactivity properties and its stability [22]. The results indicate that the size of the L. acidophilus capsules increased after coating by fish gelatin. Compared to smaller microcapsules, larger capsules provide higher protection against the core material in the food systems [16]. The zeta potential values of encapsulated L. acidophilus in alginate/fish gelatin ranged from −13.5 to −26.1 mV (Table 1). The high zeta potential of colloidal particles improves the physical stability and the electrostatic repulsion force of the system. Several factors, including pH, type, and concentration of carriers, affect the zeta potential value and surface charge [23].

3.2. Viability of Encapsulated L. acidophilus during Baking and Storage

The survival of L. acidophilus (log CFU/g) in bread before and after encapsulation in alginate/fish gelatin during the baking process and 7 days storage are presented in Table 2. The survival of L. acidophilus in all samples finally may be expected to decrease due to the high temperature during baking [24]. The results indicated that bread baking at 175 °C for 6 min reduced the viable cell count of L. acidophilus by 3.95–6.51 log CFU/g. However, the reduction in L. acidophilus during baking was much lower in the encapsulated cells in alginate/fish gelatin 1.5 and 3%, which might be attributed to the heat-protective effects of alginate and fish gelatin on the L. acidophilus cells. The survival of probiotics in bread during baking and storage is significantly influenced by the incorporated probiotic strains and physicochemical properties of capsule materials [4]. In a similar study, Zhang et al. [4] observed that the survival of L. plantarum significantly decreased to 104~5 CFU/g after bread baking at 180 °C for 5 min. Our results agree with Thang et al. [25], showing the viability of L. acidophilus encapsulated in a combination of alginate and xanthan gum was decreased by 3.64 log CFU/g during baking compared to non-capsulated, which was about reduced 5 logs CFU/g.
Re-growth of L. acidophilus was observed during the 7-day storage of bread. The bread matrix is an appropriate environment for the growth of probiotic bacteria because of the abundance of nutrients for bacterial. However, the increase in probiotic bacteria counts during the first day was insignificant (p > 0.05). This lag phase indicates that surviving cells need time to adapt to the new condition and cellular damage recovery [26]. After this lag phase, the viable counts of L. acidophilus increased by 0.5–1.5 in 4-day storage. The viability of L. acidophilus encapsulated by alginate/fish gelatin 1.5 and 3% achieved the suggested concentration (106 CFU/g) for probiotic food products. After 7-day storage, encapsulation of L. acidophilus by alginate as the single carrier and in combination with fish gelatin (0.5, 1.5, and 3%) increased the viability by about 1 and 1.5–3 log cycles, respectively. The study of Trabelsi et al. [20] indicated that the protective effect of alginate in combination with polymer compounds on the L. plantarum viability showed better results than using alginate alone during 35 days of storage at 4 °C.

3.3. Hardness and Staling Rate

The effects of free and encapsulated L. acidophilus in alginate individually and in combination with fish gelatin at 0.5, 1.5, and 3% on hardness and staling rate of bread during storage are shown in Figure 1a,c. The hardness of bread significantly increased during 7-day storage. However, fish gelatin decreased crumb hardness, in which the crumb hardness with encapsulated L. acidophilus in alginate/fish gelatin 3% was 32.2% less than that of control bread after 7-day storage. This result was probably related to more moisture content and a larger specific volume of bread caused by the increment of fish gelatin (Figure 1b and Figure 2). The staling rate of bread containing encapsulated L. acidophilus in alginate/fish gelatin 0.5, 1.5, and 3% decreased by 19.5, 25.8, and 31.7%, respectively. It appears that the weakening effect of hydrocolloids on the starch structure of bread leads to a decrease in crumb resistance and better water retention and distribution. A similar study has presented that some hydrocolloids could also reduce the hardness during bread storage [27]. By preferential binding hydrocolloids to starch, retrogradation of amylopectin is inhibited, thus hardening is postponed [28]. In a similar study, Yu et al. [11] observed that the hardness of both fresh and stored bread significantly decreased with the addition of pigskin gelatin (1%) in bread, achieving a decrease (20.8%) in staling rate for bread after 7 days of storage.

3.4. Moisture Content

Moisture loss, distribution of moisture between the crystalline and amorphous zone, and hardness must participate in the bread staling process [29]. The moisture content of bread supplemented with encapsulated L. acidophilus in different matrices during storage is shown in Figure 1b. The highest moisture content was found in the bread supplemented with encapsulated L. acidophilus in alginate/fish gelatin 3% matrix, followed by the alginate/fish gelatin 1.5% matrix. These finds were ascribed to the water-holding capacity of the fish gelatin. The jelly texture of fish gelatin allows it to keep the water in its matrix and have more water throughout the heating process. Gelatin demonstrates barrier capabilities to prevent the removal of water during the baking process by making water molecular hydrogen bonds, which make them more effective to avoid weight loss in the final product [30]. Lafarga et al. [31] similarly found that chitosan generated from marine shellfishery byproducts improved the moisture content for fresh bread and decreased moisture content after 5 days of storage.

3.5. Oven Spring and Specific Volume

Figure 2 illustrates the oven spring and specific volume values of bread supplemented with encapsulated L. acidophilus in different matrices. The results indicated that the oven spring and specific volume values of bread ranged from 1.05 to 1.58 cm and 5.38 to 6.79 cm3/g, respectively. As shown in Figure 2, the addition of alginate-encapsulated L. acidophilus to bread had no significant effect on both the oven spring and specific volume index (p > 0.05). However, these values were significantly (p < 0.05) affected by the addition of alginate/fish gelatin-encapsulated L. acidophilus, indicating the positive effect of fish gelatin for improvement of oven spring and specific volume values of bread. The extensive interaction with fish gelatin due to hydroxyl groups bonding with hydrogen on water may allow the dough to tolerate the significant increases in water absorption, leading to increased volume. The rise in oven spring and specific volume values of bread could be due to increased instability of the gluten–starch network, dough strength, and gas retention capacity [4,32]. Yu et al. [11] reported the bread volume significantly enhanced (p < 0.05) with the increment of 1% gelatin pigskin, which depends on the gas holding capacity of dough.

3.6. Internal Texture Structure

Figure 3 crumb images of the bread samples and the binarized images are used to compute the morphological characterizations of the internal texture structures. Moreover, the image analysis results of crumb structures (porosity, cell average area, and cell density) of bread supplemented with encapsulated L. acidophilus in different matrices are shown in Table 3. Compared to the control sample, bread supplemented with alginate-encapsulated L. acidophilus had a similar porosity and a lower cell average. Fish gelatin had a favorable influence on the specific volume value of bread, which relies on the gas-holding capacity of dough. The enhanced gas-holding capacity resulted in higher porosity in the bread supplemented by fish gelatin, higher cell density, and a smaller cell area. The density and size of the gas cells could lead to enormous textural and sensory attributes of the bread [11]. As shown in Figure 3, the size and height of the bread are increased by the addition of fish gelatin, which agrees with the obtained results of the oven spring and specific volume in the previous section (Section 3.5). A dual mechanism can explain gas cell stabilization at the molecular level: the gluten–starch matrix and thin liquid lamellae stabilized by adsorbed surface-active ingredients (proteins and lipids) at the gas–liquid interface. The former is the initial stabilizing factor to expand gas cells against coalescence and disproportionation [33,34].

4. Conclusions

The bread baking significantly decreased the survival of L. acidophilus to about 4.5 logs CFU/g in bread. The survival of encapsulated L. acidophilus during baking and storage is entirely affected by the composition of the capsule’s matrix. Encapsulation of probiotic cells by alginate/fish gelatin can increase their viability by 2.49 and 3.07 log CFU/g during baking and 7 days of storage, respectively. The alginate/fish gelatin 3% matrix exhibited the highest protective effect on L. acidophilus cells during baking and storage of bread. Fish gelatin as a second layer carrier of the bacteria had a positive effect on improving the technical quality of bread. Overall, the findings suggest encapsulation of L. acidophilus in alginate/fish gelatin capsule has great potential to improve probiotic bacteria’s survival during baking and storage and serves as an effective bread enhancer.

Author Contributions

Conceptualization, M.H.; data curation and methodology, N.M. and A.Z.J.; formal analysis, N.M. and Z.H.; investigation, M.H., A.Z.J. and Z.H.; writing—original draft preparation, M.H., N.M. and A.Z.J.; writing—review and editing, M.H. and A.M.K.; validation, visualization, and supervision, A.M., M.H. and A.M.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available on request from the corresponding authors.

Conflicts of Interest

The authors declare no conflict of interest related to the content of this manuscript.

References

  1. Soukoulis, C.; Yonekura, L.; Gan, H.-H.; Behboudi-Jobbehdar, S.; Parmenter, C.; Fisk, I. Probiotic edible films as a new strategy for developing functional bakery products: The case of pan bread. Food Hydrocoll. 2014, 39, 231–242. [Google Scholar] [CrossRef]
  2. Vallejo-Castillo, V.; Rodríguez-Stouvenel, A.; Martínez, R.; Bernal, C. Development of alginate-pectin microcapsules by the extrusion for encapsulation and controlled release of polyphenols from papaya (Carica papaya L.). J. Food Biochem. 2020, 44, e13331. [Google Scholar] [CrossRef]
  3. De Souza, E.L.; De Albuquerque, T.M.R.; Santos, A.; Massa, N.M.L.; Alves, J.L.D.B. Potential interactions among phenolic compounds and probiotics for mutual boosting of their health-promoting properties and food functionalities—A review. Crit. Rev. Food Sci. Nutr. 2018, 59, 1645–1659. [Google Scholar] [CrossRef]
  4. Zhang, L.; Taal, M.A.; Boom, R.M.; Chen, X.D.; Schutyser, M.A. Effect of baking conditions and storage on the viability of Lactobacillus plantarum supplemented to bread. LWT 2018, 87, 318–325. [Google Scholar] [CrossRef]
  5. Zhang, L.; Chen, X.D.; Boom, R.M.; Schutyser, M.A. Survival of encapsulated Lactobacillus plantarum during isothermal heating and bread baking. LWT 2018, 93, 396–404. [Google Scholar] [CrossRef] [Green Version]
  6. Pitigraisorn, P.; Srichaisupakit, K.; Wongpadungkiat, N.; Wongsasulak, S. Encapsulation of Lactobacillus acidophilus in moist-heat-resistant multilayered microcapsules. J. Food Eng. 2017, 192, 11–18. [Google Scholar] [CrossRef]
  7. Krasaekoopt, W.; Bhandari, B.; Deeth, H. Evaluation of encapsulation techniques of probiotics for yogurt. Int. Dairy J. 2003, 13, 3–13. [Google Scholar] [CrossRef]
  8. Mandal, S.; Puniya, A.; Singh, K. Effect of alginate concentrations on survival of microencapsulated Lactobacillus casei NCDC-298. Int. Dairy J. 2006, 16, 1190–1195. [Google Scholar] [CrossRef]
  9. Razavi, M.S.; Golmohammadi, A.; Nematollahzadeh, A.; Fiori, F.; Rovera, C.; Farris, S. Preparation of cinnamon essential oil emulsion by bacterial cellulose nanocrystals and fish gelatin. Food Hydrocoll. 2020, 109, 106111. [Google Scholar] [CrossRef]
  10. Goudoulas, T.; Germann, N. Phase transition kinetics and rheology of gelatin-alginate mixtures. Food Hydrocoll. 2017, 66, 49–60. [Google Scholar] [CrossRef]
  11. Yu, W.; Xu, D.; Li, D.; Guo, L.; Su, X.; Zhang, Y.; Wu, F.; Xu, X. Effect of pigskin-originated gelatin on properties of wheat flour dough and bread. Food Hydrocoll. 2019, 94, 183–190. [Google Scholar] [CrossRef]
  12. Tebben, L.; Li, Y. Effect of xanthan gum on dough properties and bread qualities made from whole wheat flour. Cereal Chem. J. 2018, 96, 263–272. [Google Scholar] [CrossRef]
  13. Moghanjougi, Z.M.; Bari, M.R.; Khaledabad, M.A.; Amiri, S.; Almasi, H. Microencapsulation of Lactobacillus acidophilus LA-5 and Bifidobacterium animalis BB-12 in pectin and sodium alginate: A comparative study on viability, stability, and structure. Food Sci. Nutr. 2021, 9, 5103–5111. [Google Scholar] [CrossRef]
  14. Zhang, L.; Huang, S.; Ananingsih, V.K.; Zhou, W.; Chen, X.D. A study on Bifidobacterium lactis Bb12 viability in bread during baking. J. Food Eng. 2013, 122, 33–37. [Google Scholar] [CrossRef]
  15. Hadidi, M.; Motamedzadegan, A.; Jelyani, A.Z.; Khashadeh, S. Nanoencapsulation of hyssop essential oil in chitosan-pea protein isolate nano-complex. LWT 2021, 144, 111254. [Google Scholar] [CrossRef]
  16. Jouki, M.; Khazaei, N.; Rashidi-Alavijeh, S.; Ahmadi, S. Encapsulation of Lactobacillus casei in quince seed gum-alginate beads to produce a functional synbiotic drink powder by agro-industrial by-products and freeze-drying. Food Hydrocoll. 2021, 120, 106895. [Google Scholar] [CrossRef]
  17. AACC International. Approved Methods of Analysis, 11th ed.; AACCI: St. Paul, MN, USA, 2010. [Google Scholar]
  18. Giri, N.A.; Sakhale, B.K. Optimization of whey protein concentrate and psyllium husk for the development of protein-fiber rich orange fleshed sweet potato (Ipomoea batatas L.) bread by using response surface methodology. J. Food Meas. Charact. 2019, 14, 425–437. [Google Scholar] [CrossRef]
  19. Mudgil, D.; Barak, S.; Khatkar, B. Optimization of bread firmness, specific loaf volume and sensory acceptability of bread with soluble fiber and different water levels. J. Cereal Sci. 2016, 70, 186–191. [Google Scholar] [CrossRef]
  20. Trabelsi, I.; Ayadi, D.; Bejar, W.; Bejar, S.; Chouayekh, H.; Ben Salah, R. Effects of Lactobacillus plantarum immobilization in alginate coated with chitosan and gelatin on antibacterial activity. Int. J. Biol. Macromol. 2014, 64, 84–89. [Google Scholar] [CrossRef]
  21. Mahmoud, M.; Abdallah, N.A.; El-Shafei, K.; Tawfik, T.N.; El-Sayed, H. Survivability of alginate-microencapsulated Lactobacillus plantarum during storage, simulated food processing and gastrointestinal conditions. Heliyon 2020, 6, e03541. [Google Scholar] [CrossRef]
  22. Li, K.; Wang, B.; Wang, W.; Liu, G.; Ge, W.; Zhang, M.; Yue, B.; Kong, M. Microencapsulation of Lactobacillus casei BNCC 134415 under lyophilization enhances cell viability during cold storage and pasteurization, and in simulated gastrointestinal fluids. LWT 2019, 116, 108521. [Google Scholar] [CrossRef]
  23. Hadidi, M.; Jafarzadeh, S.; Ibarz, A. Modified mung bean protein: Optimization of microwave-assisted phosphorylation and its functional and structural characterizations. LWT 2021, 151, 112119. [Google Scholar] [CrossRef]
  24. Perdana, J.; Bereschenko, L.; Fox, M.B.; Kuperus, J.H.; Kleerebezem, M.; Boom, R.M.; Schutyser, M.A. Dehydration and thermal inactivation of Lactobacillus plantarum WCFS1: Comparing single droplet drying to spray and freeze drying. Food Res. Int. 2013, 54, 1351–1359. [Google Scholar] [CrossRef]
  25. Thang, T.D.; Quyen, L.T.H.; Hang, H.T.T.; Luan, N.T.; KimThuy, D.T.; Lieu, D.M. Survival Survey of Lactobacillus acidophilus in additional probiotic bread. Turk. J. Agric.-Food Sci. Technol. 2019, 7, 588–592. [Google Scholar] [CrossRef] [Green Version]
  26. Huang, S.; Yang, Y.; Fu, N.; Qin, Q.; Zhang, L.; Chen, X.D. Calcium-aggregated milk: A potential new option for improving the viability of lactic acid bacteria under heat stress. Food Bioprocess Technol. 2014, 7, 3147–3155. [Google Scholar] [CrossRef]
  27. Guarda, A.; Rosell, C.M.; Benedito, C.; Galotto, M. Different hydrocolloids as bread improvers and antistaling agents. Food Hydrocoll. 2004, 18, 241–247. [Google Scholar] [CrossRef]
  28. Collar, C.; Martínez, J.C.; Rosell, C.M. Lipid binding of fresh and stored formulated wheat breads. Relationships with dough and bread technological performance. Food Sci. Technol. Int. 2001, 7, 501–510. [Google Scholar] [CrossRef]
  29. Rosell, C.; Rojas, J.; De Barber, C.B. Influence of hydrocolloids on dough rheology and bread quality. Food Hydrocoll. 2001, 15, 75–81. [Google Scholar] [CrossRef]
  30. Sow, L.C.; Toh, N.Z.Y.; Wong, C.W.; Yang, H. Combination of sodium alginate with tilapia fish gelatin for improved texture properties and nanostructure modification. Food Hydrocoll. 2019, 94, 459–467. [Google Scholar] [CrossRef]
  31. Lafarga, T.; Gallagher, E.; Walsh, D.; Valverde, J.; Hayes, M. Chitosan-containing bread made using marine shellfishery byproducts: Functional, bioactive, and quality assessment of the end product. J. Agric. Food Chem. 2013, 61, 8790–8796. [Google Scholar] [CrossRef] [PubMed]
  32. Shittu, T.A.; Aminu, R.A.; Abulude, E.O. Functional effects of xanthan gum on composite cassava-wheat dough and bread. Food Hydrocoll. 2009, 23, 2254–2260. [Google Scholar] [CrossRef]
  33. Lamacchia, C.; Landriscina, L.; Severini, C.; Caporizzi, R.; Derossi, A. Characterizing the rheological and bread-making properties of wheat flour treated by “Gluten FriendlyTM” technology. Foods 2021, 10, 751. [Google Scholar] [CrossRef] [PubMed]
  34. Turbin-Orger, A.; Boller, E.; Chaunier, L.; Chiron, H.; Della Valle, G.; Réguerre, A.-L. Kinetics of bubble growth in wheat flour dough during proofing studied by computed X-ray micro-tomography. J. Cereal Sci. 2012, 56, 676–683. [Google Scholar] [CrossRef]
Foods 10 02215 g001 550
Figure 1. (a) The hardness, (b) moisture content, and (c) staling rate bread supplemented with encapsulated L. acidophilus in different matrices during storage. Means ± SD with different letters in the same column represent significantly different (p > 0.05).
Figure 1. (a) The hardness, (b) moisture content, and (c) staling rate bread supplemented with encapsulated L. acidophilus in different matrices during storage. Means ± SD with different letters in the same column represent significantly different (p > 0.05).
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Foods 10 02215 g002 550
Figure 2. Oven spring and specific volume of bread supplemented with encapsulated L. acidophilus in different matrices. Means ± SD with different letters in the same column or line represent significantly different (p > 0.05).
Figure 2. Oven spring and specific volume of bread supplemented with encapsulated L. acidophilus in different matrices. Means ± SD with different letters in the same column or line represent significantly different (p > 0.05).
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Foods 10 02215 g003 550
Figure 3. The morphological profiles of cell structure from bread supplemented with encapsulated L. acidophilus in different matrices.
Figure 3. The morphological profiles of cell structure from bread supplemented with encapsulated L. acidophilus in different matrices.
Foods 10 02215 g003
Table
Table 1. Encapsulation efficiency, particle size, and zeta potential of capsules with different matrices.
Table 1. Encapsulation efficiency, particle size, and zeta potential of capsules with different matrices.
SampleEncapsulation Efficiency (%)Particle Size (µm)Zeta Potential (mV)
Alginate92.30 ± 3.18 d389.8 ± 20.9 d−13.5 ± 2.2 c
Alginate + Gelatin 0.5%95.42 ± 1.36 c569.3 ± 36.9 c−17.3 ± 1.4 b
Alginate + Gelatin 1.5%96.33 ± 2.45 b682.1 ± 0.05 b−21.0 ± 2.5 a
Alginate + Gelatin 3%98.68 ± 1.97 a736.5 ± 0.04 a−21.6 ± 3.1 a
Means ± SD in the same column with different superscripts are significantly different (p > 0.05).
Table
Table 2. The survival of L. acidophilus in bread before and after encapsulation in alginate/fish gelatin during the baking process and 7 days of storage (log CFU/g).
Table 2. The survival of L. acidophilus in bread before and after encapsulation in alginate/fish gelatin during the baking process and 7 days of storage (log CFU/g).
SampleStorage (Day)
DoughAfter Baking147
Control9.40 ± 0.29 a,A2.89 ± 0.13 c,D2.74 ± 0.14 c,D3.45 ± 0.16 c,C4.59 ± 0.11 c,B
Alginate9.22 ± 0.24 b,A4.43 ± 0.14 b,C4.36 ± 0.26 b,C5.28 ± 0.25 b,B5.44 ± 0.22 b,B
Alginate + Gelatin 0.5%9.35 ± 0.31 a,A4.37 ± 0.19 b,D4.20 ± 0.28 b,D5.15 ± 0.26 b,C5.57 ± 0.15 b,B
Alginate + Gelatin 1.5%9.19 ± 0.12 b,A5.21 ± 0.25 a,D5.19 ± 0.15 a,D6.25 ± 0.12 a,C7.82 ± 0.31 a,B
Alginate + Gelatin 3%9.33 ± 0.14 a,A5.38 ± 0.34 a,D5.25 ± 0.24 a,D6.42 ± 0.16 a,C7.66 ± 0.24 a,B
Means followed by the different lowercase letters in a column and capital letters on the lines are significantly different (p < 0.05).
Table
Table 3. Morphological characterizations of crumb structures of bread supplemented with encapsulated L. acidophilus in different matrices.
Table 3. Morphological characterizations of crumb structures of bread supplemented with encapsulated L. acidophilus in different matrices.
SamplePorosity (%)Cell Average Area (mm2)Cell Density (Cells/cm2)
Control30.49 ± 3.11 d0.69 ± 0.06 d37.36± 4.24 c
Alginate31.25 ± 1.89 d0.60 ± 0.03 c41.96 ± 2.16 b
Alginate + Gelatin 0.5%34.73 ± 2.05 c0.55 ± 0.07 b,c43.01 ± 5.50 b
Alginate + Gelatin 1.5%38.19 ± 3.64 b0.51 ± 0.05 b47.83 ± 2.95 a
Alginate + Gelatin 3%41.25 ± 3.37 a0.43 ± 0.04 a48.20 ± 3.46 a
Means ± SD with different letter in the same column represent significantly different (p > 0.05).
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Hadidi, M.; Majidiyan, N.; Jelyani, A.Z.; Moreno, A.; Hadian, Z.; Mousavi Khanegah, A. Alginate/Fish Gelatin-Encapsulated Lactobacillus acidophilus: A Study on Viability and Technological Quality of Bread during Baking and Storage. Foods 2021, 10, 2215. https://doi.org/10.3390/foods10092215

AMA Style

Hadidi M, Majidiyan N, Jelyani AZ, Moreno A, Hadian Z, Mousavi Khanegah A. Alginate/Fish Gelatin-Encapsulated Lactobacillus acidophilus: A Study on Viability and Technological Quality of Bread during Baking and Storage. Foods. 2021; 10(9):2215. https://doi.org/10.3390/foods10092215

Chicago/Turabian Style

Hadidi, Milad, Nava Majidiyan, Aniseh Zarei Jelyani, Andrés Moreno, Zahra Hadian, and Amin Mousavi Khanegah. 2021. "Alginate/Fish Gelatin-Encapsulated Lactobacillus acidophilus: A Study on Viability and Technological Quality of Bread during Baking and Storage" Foods 10, no. 9: 2215. https://doi.org/10.3390/foods10092215

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