Potential of cocoa powder and dark chocolate in protecting Gram-negative probiotic Escherichia coli Nissle 1917
DOI:
https://doi.org/10.5327/fst.483Palavras-chave:
Escherichia coli Nissle 1917, Gram-negative probiotics, Lactobacillus, probiotic chocolate, in vitro digestion, colonic fermentationResumo
Probiotic viability is affected by many factors, including the carrier food, processing, storage, and harsh gastrointestinal conditions. Chocolate has shown some potential to protect a wide range of Gram-positive probiotics under such conditions. In this study, Escherichia coli Nissle 1917, a typical Gram-negative probiotic strain, was encapsulated using various cocoa powder formulations and incorporated into the chocolate. The encapsulation efficiency, heat resistance, viability during storage, in vitro gastrointestinal digestion, and colonic fermentation were evaluated. Gram-positive strain Lactobacillus rhamnosus GG was used for comparison. Encapsulation in the combination of cocoa powder and sucrose presented the highest and satisfactory efficiency for both strains, respectively. As a result, good storage stabilities of both encapsulated strains were achieved when they were added to dark chocolate (70% cocoa) and stored at 4 °C or room temperature for 30 days. However, during the in vitro gastrointestinal digestion and colonic fermentation of chocolates enriched with these probiotics, the Gram-positive probiotic L. rhamnosus GG had a better performance than the Gram-negative probiotic E. coli Nissle 1917. Nevertheless, this study demonstrated a satisfactory maintenance of the encapsulated Gram-negative probiotic E. coli Nissle 1917 in chocolate up to 48 h of colonic fermentation.
Downloads
Referências
Afoakwa, E. O., Paterson, A., & Fowler, M. (2007). Factors influencing rheological and textural qualities in chocolate – a review. Trends in Food Science & Technology, 18(6), 290–298. https://doi.org/10.1016/j.tifs.2007.02.002
Afoakwa, E. O., Paterson, A., Fowler, M., & Vieira, J. (2008). Particle size distribution and compositional effects on textural properties and appearance of dark chocolates. Journal of Food Engineering, 87(2), 181–190. https://doi.org/10.1016/j.jfoodeng.2007.11.025
Ajlouni, S., Ranadheera, C. S., & Chua, E. L. (2021). Encapsulation increases the in vitro bioaccessibility of probiotics in yoghurt. International Journal of Dairy Technology, 74(1), 118–127. https://doi.org/10.1111/1471-0307.12746
Carvalho, N. M., Oliveira, D. L., Dib Saleh, M. A., Pintado, M., & Madureira, A. R. (2021). Preservation of human gut microbiota inoculums for in vitro fermentations studies. Fermentation, 7(1), Article 14. https://doi.org/10.3390/fermentation7010014
Chen, Q., Zhu, Z., Wang, J., Lopez, A. I., Li, S., Kumar, A., Yu, F., Chen, H., Cai, C., & Zhang, L. (2017). Probiotic E. coli Nissle 1917 biofilms on silicone substrates for bacterial interference against pathogen colonization. Acta Biomaterialia, 50, 353–360. http://doi.org/10.1016/j.actbio.2017.01.011
Darwish, M. S., Abou-Zeid, N. A., Khojah, E., Al Jumayi, H. A., Alshehry, G. A., Algarni, E. H., & Elawady, A. A. (2022). Supplementation of Labneh with Passion Fruit Peel Enhanced Survival of E. coli Nissle 1917 during Simulated Gastrointestinal Digestion and Adhesion to Caco-2 Cells. Foods, 11(11), Article 1663. https://doi.org/10.3390/foods11111663
Didar, Z. (2020). Characterization of white chocolate enriched with free or encapsulated pomegranate extract. Journal of Nutrition, Fasting and Health, 8(4), 302–309. https://doi.org/10.22038/jnfh.2020.50603.1281
Doherty, S. B., Auty, M. A., Stanton, C., Ross, R. P., Fitzgerald, G. F., & Brodkorb, A. (2012). Survival of entrapped Lactobacillus rhamnosus GG in whey protein micro-beads during simulated ex vivo gastro-intestinal transit. International Dairy Journal, 22(1), 31–43. https://doi.org/10.1016/j.idairyj.2011.06.009
Erdem, Ö., Gültekin-Özgüven, M., Berktaş, I., Erşan, S., Tuna, H. E., Karadağ, A., Özçelik, B., Güneş, G., & Cutting, S. M. (2014). Development of a novel synbiotic dark chocolate enriched with Bacillus indicus HU36, maltodextrin and lemon fiber: Optimization by response surface methodology. LWT - Food Science and Technology, 56(1), 187–193. https://doi.org/10.1016/j.lwt.2013.10.020
Fávaro-Trindade, C. S., & Grosso, C. R. F. (2002). Microencapsulation of L. acidophilus (La-05) and B. lactis (Bb-12) and evaluation of their survival at the pH values of the stomach and in bile. Journal of Microencapsulation, 19(4), 485–494. https://doi.org/10.1080/02652040210140715
He, C., Sampers, I., & Raes, K. (2021). Dietary fiber concentrates recovered from agro-industrial by-products: Functional properties and application as physical carriers for probiotics. Food Hydrocolloids, 111, Article 106175. https://doi.org/10.1016/j.foodhyd.2020.106175
Helwig, U., Lammers, K. M., Rizzello, F., Brigidi, P., Rohleder, V., Caramelli, E., Gionchetti, P., Schrezenmeir, J., Foelsch, U. R., & Schreiber, S. (2006). Lactobacilli, bifidobacteria and E. coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World Journal of Gastroenterology, 12(37), 5978–5986. https://doi.org/10.3748/wjg.v12.i37.5978
Henker, J., Laass, M. W., Blokhin, B. M., Maydannik, V. G., Bolbot, Y. K., Elze, M., Wolff, C., Schreiner, A., & Schulze, J. (2008). Probiotic Escherichia coli Nissle 1917 versus placebo for treating diarrhea of greater than 4 days duration in infants and toddlers. The Pediatric Infectious Disease Journal, 27(6), 494–499. https://doi.org/10.1097/inf.0b013e318169034c
Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., Morelli, L., Canani, R. B., Flint, H. J., Salminen, S., Calder, P. C., & Sanders, M E. (2014). Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology, 11(8), 506–514. https://doi.org/10.1038/nrgastro.2014.66
Hossain, M. N., Ranadheera, C. S., Fang, Z., & Ajlouni, S. (2021). Impact of encapsulating probiotics with cocoa powder on the viability of probiotics during chocolate processing, storage, and in vitro gastrointestinal digestion. Journal of Food Science, 86(5), 1629–1641. https://doi.org/10.1111/1750-3841.15695
Hossain, M. N., Ranadheera, C. S., Fang, Z., & Ajlouni, S. (2022a). Interaction between chocolate polyphenols and encapsulated probiotics during in vitro digestion and colonic fermentation. Fermentation, 8(6), Article 253. https://doi.org/10.3390/fermentation8060253
Hossain, M. N., Ranadheera, C. S., Fang, Z., & Ajlouni, S. (2022b). Production of short chain fatty acids and vitamin B12 during the in-vitro digestion and fermentation of probiotic chocolate. Food Bioscience, 47, Article 101682. https://doi.org/10.1016/j.fbio.2022.101682
Hossain, M. N., Ranadheera, C. S., Fang, Z., Hutchinson, G., & Ajlouni, S. (2021). Protecting the viability of encapsulated Lactobacillus rhamnosus LGG using chocolate as a carrier. Emirates Journal of Food and Agriculture, 33(8), 647–656. https://doi.org/10.9755/ejfa.2021.v33.i8.2740
Kalantarmahdavi, M., Khanzadi, S., & Salari, A. (2021). Edible films incorporating with Lactobacillus plantarum based on sourdough, wheat flour, and gelatin: films characterization and cell viability during storage and simulated gastrointestinal condition. Starch‐Stärke, 73(9–10), Article 2000268. https://doi.org/10.1002/star.202000268
Kaltsa, O., Alibade, A., Bozinou, E., Makris, D. P., & Lalas, S. I. (2021). Encapsulation of Moringa oleifera extract in Ca-alginate chocolate beads: Physical and antioxidant properties. Journal of Food Quality, 2021, Article 5549873. https://doi.org/10.1155/2021/5549873
Kandasamy, S., Vlasova, A. N., Fischer, D. D., Chattha, K. S., Shao, L., Kumar, A., Langel, S. N., Rauf, A., Huang, H.-C., Rajashekara, G., & Saif, L. J. (2017). Unraveling the differences between gram-positive and gram-negative probiotics in modulating protective immunity to enteric infections. Frontiers in Immunology, 8, Article 334. https://doi.org/10.3389/fimmu.2017.00334
Kemsawasd, V., Chaikham, P., & Rattanasena, P. (2016). Survival of immobilized probiotics in chocolate during storage and with an in vitro gastrointestinal model. Food Bioscience, 16, 37–43. https://doi.org/10.1016/j.fbio.2016.09.001
Lasta, E. L., Ronning, E. S. P., Dekker, R. F., & Cunha, M. A. A. (2021). Encapsulation and dispersion of Lactobacillus acidophilus in a chocolate coating as a strategy for maintaining cell viability in cereal bars. Scientific Reports, 11(1), Article 20550. https://doi.org/10.1038/s41598-021-00077-0
Maltby, R., Leatham-Jensen, M. P., Gibson, T., Cohen, P. S., & Conway, T. (2013). Nutritional basis for colonization resistance by human commensal Escherichia coli strains HS and Nissle 1917 against E. coli O157:H7 in the mouse intestine. PLoS One, 8(1), Article e53957. https://doi.org/10.1371/journal.pone.0053957
Mandal, S., Hati, S., Puniya, A. K., Singh, R., & Singh, K. (2013). Development of synbiotic milk chocolate using encapsulated Lactobacillus casei NCDC 298. Journal of Food Processing and Preservation, 37(5), 1031–1037. https://doi.org/10.1111/j.1745-4549.2012.00759.x
Marcial-Coba, M. S., Saaby, L., Knøchel, S., & Nielsen, D. S. (2019). Dark chocolate as a stable carrier of microencapsulated Akkermansia muciniphila and Lactobacillus casei. FEMS Microbiology Letters, 366(2), Article fny290. https://doi.org/10.1093/femsle/fny290
Martinsen, T. C., Bergh, K., & Waldum, H. L. (2005). Gastric juice: a barrier against infectious diseases. Basic & Clinical Pharmacology & Toxicology, 96(2), 94–102. https://doi.org/10.1111/j.1742-7843.2005.pto960202.x
Minekus, M., Alminger, M., Alvito, P., Ballance, S., Bohn, T., Bourlieu, C., Carrière, F., Boutrou, R., Corredig, M., Dupont, D., Dufour, C., Egger, L., Golding, M., Karakaya, S., Kirkhus, B., Le Feunteun, S., Lesmes, U., Macierzanka, A., Mackie, A., … Brodkorb, A. (2014). A standardised static in vitro digestion method suitable for food–an international consensus. Food & Function, 5(6), 1113–1124. https://doi.org/10.1039/C3FO60702J
Muhammad, Z., Ramzan, R., Zhang, R., & Zhang, M. (2021). Resistant starch-based edible coating composites for spray-dried microencapsulation of Lactobacillus acidophilus, comparative assessment of thermal protection, in vitro digestion and physicochemical characteristics. Coatings, 11(5), Article 587. https://doi.org/10.3390/coatings11050587
Rietschel, E. T., Brade, H., Holst, O., Brade, L., Müller-Loennies, S., Mamat, U., Zähringer, U., Beckmann, F., Seydel, U., Brandenburg, K., Ulmer, A. J., Mattern, T., Heine, H., Schletter, J., Loppnow, H., Schönbeck, U., Flad, H.-D., Hauschildt, S., Schade, U. F., … Schumann, R. R. (1996). Bacterial endotoxin: chemical constitution, biological recognition, host response, and immunological detoxification. In E. T. Rietschel & H. Wagner (Eds.), Pathology of Septic Shock (pp. 39–81). Springer. https://doi.org/10.1007/978-3-642-80186-0_3
Satapathy, M., Quereshi, D., Nguyen, T. T. H., Pani, D., Mohanty, B., Anis, A., Maji, S., Kim, D., Sarkar, P., & Pal, K. (2019). Preparation and characterization of cocoa butter and whey protein isolate based emulgels for pharmaceutical and probiotics delivery applications. Journal of Dispersion Science and Technology, 41(3), 426–440. https://doi.org/10.1080/01932691.2019.1583577
Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T. A., Stange, E. F., & Fellermann, K. (2007). Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infection and Immunity, 75(5), 2399–2407. https://doi.org/10.1128/iai.01563-06
Schultz, M. (2008). Clinical use of E. coli Nissle 1917 in inflammatory bowel disease. Inflammatory Bowel Diseases, 14(7), 1012–1018. https://doi.org/10.1002/ibd.20377
Silva, K. K. P., Queirós, M. S., Ribeiro, A. P. B., & Gigante, M. L. (2022). Modified milk fat as encapsulating material for the probiotic microorganism Lactobacillus acidophilus LA3. International Dairy Journal, 125, Article 105237. https://doi.org/10.1016/j.idairyj.2021.105237
Silva, M. P., Tulini, F. L., Marinho, J. F. U., Mazzocato, M. C., De Martinis, E. C. P., Luccas, V., & Favaro-Trindade, C. S. (2017). Semisweet chocolate as a vehicle for the probiotics Lactobacillus acidophilus LA3 and Bifidobacterium animalis subsp. lactis BLC1: Evaluation of chocolate stability and probiotic survival under in vitro simulated gastrointestinal conditions. LWT, 75, 640–647. https://doi.org/10.1016/j.lwt.2016.10.025
Smith, J. L. (2003). The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. Journal of Food Protection, 66(7), 1292–1303. https://doi.org/10.4315/0362-028x-66.7.1292
Yao, M., Xie, J., Du, H., McClements, D. J., Xiao, H., & Li, L. (2020). Progress in microencapsulation of probiotics: A review. Comprehensive Reviews in Food Science and Food Safety, 19(2), 857–874. https://doi.org/10.1111/1541-4337.12532
Yu, H., Shang, L., Zeng, X., Li, N., Liu, H., Cai, S., Huang, S., Wang, G., Wang, Y., Song, Q., & Qiao, S. (2018). Risks related to high-dosage recombinant antimicrobial peptide microcin J25 in mice model: intestinal microbiota, intestinal barrier function, and immune regulation. Journal of Agricultural and Food Chemistry, 66(43), 11301–11310. https://doi.org/10.1021/acs.jafc.8b03405
