Survivability of alginate-microencapsulated Lactobacillus plantarum during storage, simulated food processing and gastrointestinal conditions

Heliyon

Volumn 6, Issue 3, 2020, Pages

  Mahmoud, Mona ^a   Abdallah, Nagwa A ^b   El Shafei, Kawther ^a   Tawfik, Nabil F ^a   El Sayed, Hoda S ^a  

^a NATIONAL RESEARCH CENTRE   (Egypt)

^b Ain Shams University   (Egypt)

Author keywords

Antimicrobial; Extrusion; Food science; Lactobacillus plantarum; Materials science; Microbiology; Microencapsulation; Sodium alginate

Indexed keywords

EID: 85081004775     PISSN: 24058440     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heliyon.2020.e03541     Document Type: Article

References (85)

1. Abd El-Salam, M.H., El-Shibiny, S., Preparation and properties of milk proteins-based encapsulated probiotics: a review. Dairy Sci. Technol. 95 (2015), 393–412.
2. Albadran, H.A., Chatzifragkou, A., Khutoryanskiy, V.V., Charalampopoulos, D., Stability of probiotic Lactobacillus plantarum in dry microcapsules under accelerated storage conditions. Food Res. Int. 74 (2015), 208–216.
3. Arena, M.P., Silvain, A., Normanno, G., Grieco, F., Drider, D., Spano, G., Fiocco, D., Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front. Microbiol. 7 (2016), 1–10.
4. Baek, Y.J., Lee, B.H., Probiotics and prebiotics as bioactive components in dairy products. Park, Y.W., (eds.) Bioactive Components of Milk and Dairy Products, 2009, 287–310 Wiley-Black well.
5. Barbosa, M.S., Todorov, S.D., Ivanova, I.V., Belguesmia, Y., Choiset, Y., Rabesona, H., Chobert, J.-M., Haertlé, T., Franco, B.D.G.M., Characterization of a two-peptide plantaricin produced by Lactobacillus plantarum MBSa4 isolated from Brazilian salami. Food Contr. 60 (2016), 103–112.
6. Bilenler, T., Karabulut, I., Candogan, K., Effects of encapsulated starter cultures on microbial and physicochemical properties of traditionally produced and heat treated sausages (sucuks). LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.) 75 (2017), 425–433.
7. Bosnea, L.A., Moschakis, T., Biliaderis, C.G., Complex coacervation as a novel microencapsulation technique to improve viability of probiotics under different stresses. Food Bioprocess Technol. 7 (2014), 2767–2781.
8. Brinques, G.B., Ayub, M.A.Z., Effect of microencapsulation on survival of Lactobacillus plantarum in simulated gastrointestinal conditions, refrigeration, and yogurt. J. Food Eng. 103 (2011), 123–128.
9. Burgain, J., Gaiani, C., Linder, M., Scher, J., Encapsulation of probiotic living cells: from laboratory scale to industrial applications. J. Food Eng. 104 (2011), 467–483.
10. Burgain, J., Scher, J., Lebeer, S., Vanderleyden, J., Cailliez-Grimal, C., Corgneau, M., Francius, G., Gaiani, C., Significance of bacterial surface molecules interactions with milk proteins to enhance microencapsulation of Lactobacillus rhamnosus GG. Food Hydrocolloids 41 (2014), 60–70.
11. Çabuk, B., Tellioğlu Harsa, Ş., Protection of Lactobacillus acidophilus NRRL-B 4495 under in vitro gastrointestinal conditions with whey protein/pullulan microcapsules. J. Biosci. Bioeng. 120 (2015), 650–656.
12. Castro, J.M., Tornadijo, M.E., Fresno, J.M., Sandoval, H., Biocheese: a food probiotic carrier. BioMed Res. Int., 2015, 2015.
13. Castro-Cislaghi, F.P. De, Silva, C.D.R.E., Fritzen-Freire, C.B., Lorenz, J.G., Sant'Anna, E.S., Bifidobacterium Bb-12 microencapsulated by spray drying with whey: survival under simulated gastrointestinal conditions, tolerance to NaCl, and viability during storage. J. Food Eng. 113 (2012), 186–193.
14. Chandramouli, V., Kailasapathy, K., Peiris, P., Jones, M., An improved method of microencapsulation and its evaluation to protect Lactobacillus spp. in simulated gastric conditions. J. Microbiol. Methods 56 (2004), 27–35.
15. Chávarri, M., Marañón, I., Ares, R., Ibáñez, F.C., Marzo, F., Villarán, C., Microencapsulation of a probiotic and prebiotic in alginate-chitosan capsules improves survival in simulated gastro-intestinal conditions. Int. J. Food Microbiol. 142 (2010), 185–189.
16. Chen, H.Y., Li, X.Y., Liu, B.J., Meng, X.H., Microencapsulation of Lactobacillus bulgaricus and survival assays under simulated gastrointestinal conditions. J. Funct. Foods 29 (2017), 248–255.
17. Chen, J., Wang, Q., Liu, C.M., Gong, J., Issues deserve attention in encapsulating probiotics: critical review of existing literature. Crit. Rev. Food Sci. Nutr. 57 (2017), 1228–1238.
18. Cook, M.T., Tzortzis, G., Charalampopoulos, D., Khutoryanskiy, V.V., Microencapsulation of probiotics for gastrointestinal delivery. J. Contr. Release 162 (2012), 56–67.
19. Corona-Hernandez, R.I., Álvarez-Parrilla, E., Lizardi-Mendoza, J., Islas-Rubio, A.R., la Rosa, L.A. de, Wall-Medrano, A., Structural stability and viability of microencapsulated probiotic bacteria: a review. Compr. Rev. Food Sci. Food Saf. 12 (2013), 614–628.
20. Das, D., Rameshbabu, A.P., Ghosh, P., Patra, P., Dhara, S., Pal, S., Biocompatible nanogel derived from functionalized dextrin for targeted delivery of doxorubicin hydrochloride to MG 63 cancer cells. Carbohydr. Polym. 171 (2017), 27–38.
21. Dehkordi, S.S., Alemzadeh, I., Vaziri, A.S., Vossoughi, A., Optimization of alginate-whey protein isolate microcapsules for survivability and release behavior of probiotic bacteria. Appl. Biochem. Biotechnol., 2019, 182–196.
22. Dianawati, D., Mishra, V., Shah, N.P., Stability of microencapsulated Lactobacillus acidophilus and Lactococcus lactis ssp. cremoris during storage at room temperature at low aw. Food Res. Int. 50 (2013), 259–265.
23. Ding, W.K., Shah, N.P., Effect of homogenization techniques on reducing the size of microcapsules and the survival of probiotic bacteria therein. J. Food Sci. 74 (2009), 231–236.
24. Divya, J.B., Varsha, K.K., Nampoothiri, K.M., Ismail, B., Pandey, A., Probiotic fermented foods for health benefits. Eng. Life Sci. 12 (2012), 377–390.
25. El-Shafei, k., Sadek, Z.I., Salem, M.M.E., Encapsulation of lactic acid bacteria to avoid the antagonism during the manufacture of probiotic soft cheese. Minufiya J. Agric. Res. 29 (2004), 1279–1293.
26. Etchepare, M. de A., Barin, J.S., Cichoski, A.J., Jacob-Lopes, E., Wagner, R., Fries, L.L.M., Menezes, C.R. de., Microencapsulation of probiotics using sodium alginate. Ciência Rural. 45 (2015), 1319–1326.
27. Fareez, I.M., Lim, S.M., Mishra, R.K., Ramasamy, K., Chitosan coated alginate-xanthan gum bead enhanced pH and thermotolerance of Lactobacillus plantarum LAB12. Int. J. Biol. Macromol. 72 (2015), 1419–1428.
28. Feucht, A., Kwak, H.S., Microencapsulation of lactic acid bacteria (LAB). Kor. J. Food Sci. Anim. Res. 33 (2013), 229–238.
29. Gåserød, O., Sannes, A., Skjåk-Bræk, G., Microcapsules of alginate-chitosan. II. A study of capsule stability and permeability. Biomaterials 20 (1999), 773–783.
30. Gbassi, G.K., Vandamme, T., Ennahar, S., Marchioni, E., Microencapsulation of Lactobacillus plantarum spp in an alginate matrix coated with whey proteins. Int. J. Food Microbiol. 129 (2009), 103–105.
31. Gibbs, B.F., Kermasha, S., Alli, I., Mulligan, C.N., Encapsulation in the food industry: a review. Int. J. Food Sci. Nutr. 50 (1999), 213–224.
32. Giraffa, G., Chanishvili, N., Widyastuti, Y., Importance of lactobacilli in food and feed biotechnology. Res. Microbiol. 161 (2010), 480–487.
33. Haghshenas, B., Abdullah, N., Nami, Y., Radiah, D., Rosli, R., Yari Khosroushahi, A., Microencapsulation of probiotic bacteria Lactobacillus plantarum 15HN using alginate-psyllium-fenugreek polymeric blends. J. Appl. Microbiol. 118 (2015), 1048–1057.
34. Homayouni, A., Azizi, A., Ehsani, M.R., Yarmand, M.S., Razavi, S.H., Effect of microencapsulation and resistant starch on the probiotic survival and sensory properties of synbiotic ice cream. Food Chem. 111 (2008), 50–55.
35. Homayouni, A., Azizi, A., Javadi, M., Mahdipour, S., Ejtahed, H., Factors influencing probiotic survival in ice cream: a review. Int. J. Dairy Sci. 7 (2012), 1–10.
36. Huq, T., Khan, A., Khan, R.A., Riedl, B., Lacroix, M., Encapsulation of probiotic bacteria in biopolymeric system. Crit. Rev. Food Sci. Nutr. 53 (2013), 909–916.
37. Ilha, E.C., Silva, T. da, Lorenz, J.G., Oliveira Rocha, G. de, Sant'Anna, E.S., Lactobacillus paracasei isolated from grape sourdough: acid, bile, salt, and heat tolerance after spray drying with skim milk and cheese whey. Eur. Food Res. Technol. 240 (2015), 977–984.
38. Kailasapathy, K., Chin, J., Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol. Cell Biol. 78 (2000), 80–88.
39. Kavitake, D., Kandasamy, S., Devi, P.B., Shetty, P.H., Recent developments on encapsulation of lactic acid bacteria as potential starter culture in fermented foods – a review. Food Biosci. 21 (2018), 34–44.
40. Kechagia, M., Basoulis, D., Konstantopoulou, S., Dimitriadi, D., Gyftopoulou, K., Skarmoutsou, N., Fakiri, E.M., Health benefits of probiotics: a review. ISRN Nutrition 2013 (2013), 1–7.
41. Kennes, C., Dubourguler, H.C., Albagnac, G., Nyns, E.-J., Citrate metabolism by Lactobacillus plantarum isolated from orange juice. J. Appl. Bacteriol. 70 (1991), 380–384.
42. Kilara, A., Panyam, D., Peptides from milk proteins and their properties. Crit. Rev. Food Sci. Nutr. 43 (2003), 607–633.
43. Krasaekoopt, W., Bhandari, B., Deeth, H., Evaluation of encapsulation techniques of probiotics for yoghurt. Int. Dairy J. 13 (2003), 3–13.
44. Kühbeck, D., Mayr, J., Häring, M., Hofmann, M., Quignard, F., Díaz Díaz, D., Evaluation of the nitroaldol reaction in the presence of metal ion-crosslinked alginates. New J. Chem. 39 (2015), 2306–2315.
45. Lee, Y., Ji, Y.R., Lee, S., Choi, M.J., Cho, Y., Microencapsulation of probiotic Lactobacillus acidophilus kbl409 by extrusion technology to enhance survival under simulated intestinal and freeze-drying conditions. J. Microbiol. Biotechnol. 29 (2019), 721–730.
46. Li, S., Walsh, H., Gokavi, S., Guo, M., Interactions between Lactobacillus acidophilus strains and the starter cultures, Lactobacillus bulgaricus and Streptococcus thermophilus during fermentation of goats’ milk. Afr. J. Biotechnol. 11 (2012), 11271–11279.
47. Li, P., Gu, Q., Zhou, Q., Complete genome sequence of Lactobacillus plantarum LZ95, a potential probiotic strain producing bacteriocins and B-group vitamin riboflavin. J. Biotechnol. 238 (2016), 52–55.
48. Liu, X., Cao, S., Zhang, X., Modulation of gut microbiota-brain Axis by probiotics, prebiotics, and diet. J. Agric. Food Chem. 63 (2015), 7885–7895.
49. Liu, H., Cui, S.W., Chen, M., li, Y., Liang, R., Xu, F., Zhong, F., Protective approaches and mechanisms of microencapsulation to the survival of probiotic bacteria during processing, storage and gastrointestinal digestion: a review. Crit. Rev. Food Sci. Nutr. 59 (2019), 2863–2878.
50. Mallesha, Shylaja R., Selvakumar, D., Jagannath, J.H., Isolation and identification of lactic acid bacteria from raw and fermented products and their antibacterial activity. J. Recent Res. Sci. Technol. 2 (2010), 42–46.
51. Maresca, D., Prisco, A. De, Storia, A., La Cirillo, T., Esposito, F., Mauriello, G., Microencapsulation of nisin in alginate beads by vibrating technology: preliminary investigation. LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.) 66 (2016), 436–443.
52. Martin, M.J., Lara-Villoslada, F., Ruiz, M.A., Morales, M.E., Effect of unmodified starch on viability of alginate-encapsulated Lactobacillus fermentum CECT5716. LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.) 53 (2013), 480–486.
53. Matejčeková, Z., Liptáková, D., Spodniaková, S., Valík, Ľ., Characterization of the growth of Lactobacillus plantarum in milk in dependence on temperature. Acta Chim. Slovaca 9 (2016), 104–108.
54. Mirzaei, H., Pourjafar, H., Homayouni, A., Effect of calcium alginate and resistant starch microencapsulation on the survival rate of Lactobacillus acidophilus La5 and sensory properties in Iranian white brined cheese. Food Chem. 132 (2012), 1966–1970.
55. Mosilhey, S.H., Influence of Different Capsule Materials on the Physiological Properties of Microencapsulated Lactobacillus acidophilus. Thesis PhD-Ingeneur, 2003, Institute of Food Technology, Faculty of Agriculture, University of Bonn, Germany Available from: http://hss.ulb.uni-bonn.de/2003/0154/0154.pdf Accessed 2012 July.
56. Moumita, S., Goderska, K., Johnson, E.M., Das, B., Indira, D., Yadav, R., Kumari, S., Jayabalan, R., Evaluation of the viability of free and encapsulated lactic acid bacteria using in-vitro gastro intestinal model and survivability studies of synbiotic microcapsules in dry food matrix during storage. LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.) 77 (2017), 460–467.
57. Muthukumarasamy, P., Allan-Wojtas, Paula, Holley, R.a., Stability of Lactobacillus reuteri in different types of microcapsules. J. Food Sci. 71 (2006), 20–24.
58. Nie, P., Li, Z., Wang, Y., Zhang, Y., Zhao, M., Luo, J., Du, S., Deng, Z., Chen, J., Wang, Y., Chen, S., Wang, L., Gut microbiome interventions in human health and diseases. Med. Res. Rev. 39 (2019), 2286–2313.
59. Nualkaekul, S., Lenton, D., Cook, M.T., Khutoryanskiy, V.V., Charalampopoulos, D., Chitosan coated alginate beads for the survival of microencapsulated Lactobacillus plantarum in pomegranate juice. Carbohydr. Polym. 90 (2012), 1281–1287.
60. Ouled-Haddar, H., Sifour, M., Idoui, T., Bouridane, H., Arid, S., Lactobacillus plantarum G1 microencapsulation enhanced its viability during storage and gastrointestinal transit. Sains Malays. 45 (2016), 1049–1055.
61. Patil, A., Disouza, J., Pawar, S., Shelf life stability of encapsulated lactic acid bacteria isolated from sheep milk thrived in different milk as natural media. Small Rumin. Res. 170 (2019), 19–25.
62. Quigley, E.M.M., Prebiotics and probiotics in digestive health. Clin. Gastroenterol. Hepatol. 17 (2019), 333–344.
63. Rajam, R., Karthik, P., Parthasarathi, S., Joseph, G.S., Anandharamakrishnan, C., Effect of whey protein - alginate wall systems on survival of microencapsulated Lactobacillus plantarum in simulated gastrointestinal conditions. J. Funct. Foods 4 (2012), 891–898.
64. Rathore, S., Desai, P.M., Liew, C.V., Chan, L.W., Heng, P.W.S., Microencapsulation of microbial cells. J. Food Eng. 116 (2013), 369–381.
65. Rokka, S., Rantamäki, P., Protecting probiotic bacteria by microencapsulation: challenges for industrial applications. Eur. Food Res. Technol. 231 (2010), 1–12.
66. Rosas-Flores, W., Ramos-Ramírez, E.G., Salazar-Montoya, J.A., Microencapsulation of Lactobacillus helveticus and Lactobacillus delbrueckii using alginate and gellan gum. Carbohydr. Polym. 98 (2013), 1011–1017.
67. Shah, N.P., Probiotic bacteria: selective enumeration and survival in dairy foods. J. Dairy Sci. 83 (2000), 894–907.
68. Shi, L.E., Li, Z.H., Li, D.T., Xu, M., Chen, H.Y., Zhang, Z.L., Tang, Z.X., Encapsulation of probiotic Lactobacillus bulgaricus in alginate'milk microspheres and evaluation of the survival in simulated gastrointestinal conditions. J. Food Eng. 117 (2013), 99–104.
69. Shori, A.B., The potential applications of probiotics on dairy and non-dairy foods focusing on viability during storage. Biocatal. Agric. Biotechnol. 4 (2015), 423–431.
70. Shori, A.B., Microencapsulation improved probiotics survival during gastric transit. HAYATI J. Biosci. 24 (2017), 1–5.
71. Sieuwerts, S., Bron, P.A., Smid, E.J., Mutually stimulating interactions between lactic acid bacteria and Saccharomyces cerevisiae in sourdough fermentation. LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.) 90 (2018), 201–206.
72. Su, R., Zhu, X.L., Fan, D.Di, Mi, Y., Yang, C.Y., Jia, X., Encapsulation of probiotic Bifidobacterium longum BIOMA 5920 with alginate-human-like collagen and evaluation of survival in simulated gastrointestinal conditions. Int. J. Biol. Macromol. 49 (2011), 979–984.
73. Suez, J., Zmora, N., Segal, E., Elinav, E., The pros, cons, and many unknowns of probiotics. Nat. Med., 25, 2019.
74. Sultana, K., Godward, G., Reynolds, N., Arumugaswamy, R., Peiris, P., Kailasapathy, K., Encapsulation of probiotic bacteria with alginate-starch and evaluation of survival in simulated gastrointestinal conditions and in yoghurt. Int. J. Food Microbiol. 62 (2000), 47–55.
75. Teoh, P.L., Mirhosseini, H., Mustafa, S., Hussin, A.S.M., Abdul Manap, M.Y., Recent approaches in the development of encapsulated delivery systems for probiotics. Food Biotechnol. 25 (2011), 77–101.
76. Trabelsi, I., Bejar, W., Ayadi, D., Chouayekh, H., Kammoun, R., Bejar, S., Salah, R. Ben., Encapsulation in alginate and alginate coated-chitosan improved the survival of newly probiotic in oxgall and gastric juice. Int. J. Biol. Macromol., 61, 2013, 36—42.
77. Tripathi, M.K., Giri, S.K., Probiotic functional foods: survival of probiotics during processing and storage. J. Funct. Foods 9 (2014), 225–241.
78. Umeki, K., Yamamoto, T., Structures of multi-branched dextrins produced by saccharifying α-amylase from starch. J. Biochem. 78 (1975), 897–903.
79. Vinderola, C.G., Mocchiutti, P., Reinheimer, J.A., Interactions among lactic acid starter and probiotic bacteria used for fermented dairy products. J. Dairy Sci. 85 (2002), 721–729.
80. Wang, S.Y., Ho, Y.F., Chen, Y.P., Chen, M.J., Effects of a novel encapsulating technique on the temperature tolerance and anti-colitis activity of the probiotic bacterium Lactobacillus kefiranofaciens M1. Food Microbiol. 46 (2015), 494–500.
81. Wheater, D.M., The characteristics of Lactobacillus plantarum, L. helveticus and L. casei. J. Gen. Microbiol. 12 (1955), 133–139.
82. Zhang, Z., Liu, Z., Tao, X., Wei, H., Characterization and sulfated modification of an exopolysaccharide from Lactobacillus plantarum ZDY2013 and its biological activities. Carbohydr. Polym. 153 (2016), 25–33.
83. Zhou, Y., Martins, E., Groboillot, a., Champagne, C., Neufeld, R.J., Spectrophotometric quantification of lactic bacteria in alginate and control of cell release with chitosan coating. J. Appl. Microbiol. 84 (1998), 342–348.
84. Zhu, X.Y., Liu, F., Review Article Probiotics as an Adjuvant Treatment in Helicobacter pylori Eradication Therapy. 2017.
85. Zisu, B., Shah, N.P., Effects of pH, temperature, supplementation with whey protein concentrate, and adjunct cultures on the production of exopolysaccharides by Streptococcus thermophilus 1275. J. Dairy Sci. 86 (2003), 3405–3415.