Cocoa Pulp as Alternative Food Matrix for Probiotic Delivery

Page: [82 - 90] Pages: 9

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Abstract

Background: For screening probiotic strains with viability and stability in non-dairy foods for health benefits, we revised all patents relating to probiotics in food.

Objective: Screening of potential probiotics from Brazilian Minas artisanal cheese and verify their survival in frozen Brazilian cocoa pulp.

Methods: Isolation and identification of the strains. The potential probiotic characterization involved gastric juice and bile resistance, antibiotic and antimicrobial activity, hydrophobicity, autoaggregation, coaggregation and adhesion assay in HT-29 cells. Organoleptic, viability and stability of probiotic strain in frozen cocoa pulp were evaluated.

Results: Fourteen strains of Lactobacillus plantarum (9), Weissella paramesenteroides (3), Lactobacillus fermentum (1), and Leuconostoc mesenteroides (1) were obtained. Most of the strains were resistant to simulated gastric acidity and bile salts. Almost all strains were sensitive to the antibiotics tested, except to ciprofloxacin and vancomycin. About 47% of the strains are potential producers of bacteriocins. High hydrophobicity was observed for four strains. Autoaggregation ranged from 8.3-72.6% and the coaggregation capacity from 5.2-60.2%. All of the assessed strains presented more than 90% of adhesion to HT-29 intestinal cells. The percentage of Salmonella inhibition in HT-29 cells ranged from 4.7-31.1%. No changes in color, aroma, and pH were observed in cocoa pulps after storage at -20 °C for 90 days.

Conclusion: Wild strains of acid lactic bacteria from cheese proved to be viable and stable in frozen Brazilian cocoa pulp. This work showed a promising application of L. plantarum isolated strains to be used with frozen cocoa pulp matrix in probiotics food industry.

Keywords: Probiotic, lactic acid bacteria, cheese, screening, cocoa, non-dairy.

Graphical Abstract

[1]
Min M, Bunt CR, Mason SL, Hussain MA. Non-dairy probiotic food products: An emerging group of functional foods. Crit Rev Food Sci Nutr 2018; 9: 1-6.
[PMID: 29630845]
[2]
Min M, Bunt CR, Mason SL, Bennett GN, Hussain MA. Effect of non-dairy food matrices on the survival of probiotic bacteria during storage. Microorganisms 2017; 5(3): 1-7.
[http://dx.doi.org/10.3390/microorganisms5030043] [PMID: 28763015]
[3]
Gawkowski D, Chikindas ML. Non-dairy probiotic beverages: the next step into human health. Benef Microbes 2013; 4(2): 127-42.
[http://dx.doi.org/10.3920/BM2012.0030] [PMID: 23271064]
[4]
Rivera-Espinoza Y, Gallardo-Navarro Y. Non-dairy probiotic products. Food Microbiol 2010; 27(1): 1-11.
[http://dx.doi.org/10.1016/j.fm.2008.06.008] [PMID: 19913684]
[5]
Ramos AM, Martins EMF, Martins ML. Salada de fruta probiótica minimamente processada, processo de obtenção e uso de probióticos em saladas de frutas minimamente processadas.BR1020120189232A2 (2015).
[6]
Tao X, Mingyong X, Qianqian G, Gaoping S. Preparation method of probiotics-fermented fruit and vegetable jam ice cream.CN103005134A (2013).
[7]
Magalhaes JT, Valadares HMS, Gonçalves DB, Granjeiro PA. P.A. Cocoa-based drink in natura with addition of probiotic.BR1020160259282 (2016).
[8]
Zhang J, Zhang X, Zhang L. Zhao Y, Niu C, Yang Z, et al.Potential probiotic characterization of Lactobacillus plantarum strains isolated from Inner Mongolia “Hurood” cheese. J Microbiol Biotechnol 2014; 24(2): 225-35.
[http://dx.doi.org/10.4014/jmb.1308.08075] [PMID: 24225370]
[9]
Park S, Ji Y, Park H, Lee K, Park H, Beck BR, et al. Evaluation of functional properties of lactobacilli isolated from Korean White Kimchi. Food Control 2016; 69: 5-12.
[http://dx.doi.org/10.1016/j.foodcont.2016.04.037]
[10]
Badrie N, Bekele F, Sikora E, Sikora M. Cocoa agronomy, quality, nutritional, and health aspects. Crit Rev Food Sci Nutr 2015; 55(5): 620-59.
[http://dx.doi.org/10.1080/10408398.2012.669428] [PMID: 24915358]
[11]
Schwan RF, Wheals AE. The microbiology of cocoa fermentation and its role in chocolate quality. Crit Rev Food Sci Nutr 2004; 44(4): 205-21.
[http://dx.doi.org/10.1080/10408690490464104] [PMID: 15462126]
[12]
Penha EM, Da Matta VM. Características físico-químicas e microbiológicas da polpa de cacau. Pesqui Agropecu Bras 1998; 33: 1945-9.
[13]
Rasolofo EA, St-Gelais D, LaPointe G, Roy D. Molecular analysis of bacterial population structure and dynamics during cold storage of untreated and treated milk. Int J Food Microbiol 2010; 138(1-2): 108-18.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2010.01.008] [PMID: 20137820]
[14]
Torriani S, Felis GE, Dellaglio F. Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA gene sequence analysis and multiplex PCR assay with recA gene-derived primers. Appl Environ Microbiol 2001; 67(8): 3450-4.
[http://dx.doi.org/10.1128/AEM.67.8.3450-3454.2001] [PMID: 11472918]
[15]
Gregoret V, Perezlindo MJ, Vinderola G, Reinheimer J, Binetti A. A comprehensive approach to determine the probiotic potential of human-derived Lactobacillus for industrial use. Food Microbiol 2013; 34(1): 19-28.
[http://dx.doi.org/10.1016/j.fm.2012.11.004] [PMID: 23498174]
[16]
Vinderola CG, Reinheimer JA. Lactic acid starter and probiotic bacteria: a comparative in vitro study of probiotic characteristics and biological barrier resistance. Food Res Int 2003; 36: 895-904.
[http://dx.doi.org/10.1016/S0963-9969(03)00098-X]
[17]
Vinderola CG, Capellini B, Villarreal F, Suárez V, Quiberoni A, Reinheimer J. Usefulness of a set of simple in vitro tests for the screening and identification of probiotic candidate strains for dairy use. Lebensm Wiss Technol 2008; 41: 1678-88.
[http://dx.doi.org/10.1016/j.lwt.2007.10.008]
[18]
Todorov SD, Leblanc JG, Franco BD. Evaluation of the probiotic potential and effect of encapsulation on survival for Lactobacillus plantarum ST16Pa isolated from papaya. World J Microbiol Biotechnol 2012; 28(3): 973-84.
[http://dx.doi.org/10.1007/s11274-011-0895-z] [PMID: 22805818]
[19]
CLSI.Clinical and Laboratory Standards Institute.Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement In: 2015. CLSI 2015; 35(3): M100-S25 (ISBN 1-56238-989-0 [Print]; ISBN 1-56238-990-4 [Electronic]).
[20]
Meira SMM, Helfer VE, Velho RV, Lopes FC, Brandelli A. Probiotic potential of Lactobacillus spp. isolated from Brazilian regional ovine cheese. J Dairy Res 2012; 79(1): 119-27.
[http://dx.doi.org/10.1017/S0022029911000884] [PMID: 23171587]
[21]
González L, Sandoval H, Sacristán N, Castro JM, Fresno JM, Tornadijo ME. Identification of lactic acid bacteria isolated from Genestoso cheese throughout ripening and study of their antimicrobial activity. Food Control 2007; 18: 716-22.
[http://dx.doi.org/10.1016/j.foodcont.2006.03.008]
[22]
Kos B, Susković J, Vuković S, Šimpraga M, Frece J, Matosić S. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 2003; 94(6): 981-7.
[http://dx.doi.org/10.1046/j.1365-2672.2003.01915.x] [PMID: 12752805]
[23]
Tulini FL, Winkelströter LK, De Martinis EC. Identification and evaluation of the probiotic potential of Lactobacillus paraplantarum FT259, a bacteriocinogenic strain isolated from Brazilian semi-hard artisanal cheese. Anaerobe 2013; 22: 57-63.
[http://dx.doi.org/10.1016/j.anaerobe.2013.06.006] [PMID: 23792229]
[24]
Brazil, Ministério da Agricultura, Pecuária e Abastecimento - Instrução Normativa n° 01, 07 Jan. 2000. Regulamento Técnico Geral para fixação dos Padrões de Identidade e Qualidade para polpa de fruta conforme consta do Anexo I desta Instrução Normativa.Diário Oficial da União, Brasília, 10 set 1999.
[25]
Guan X, Xu Q, Zheng Y, Qian L, Lin B. Screening and characterization of lactic acid bacterial strains that produce fermented milk and reduce cholesterol levels. Braz J Microbiol 2017; 48(4): 730-9.
[http://dx.doi.org/10.1016/j.bjm.2017.02.011] [PMID: 28625768]
[26]
Fialho TL, Carrijo LC, Magalhães Júnior MJ, Baracat-Pereira MC, Piccoli RH, de Abreu LR. Extraction and identification of antimicrobial peptides from the Canastra artisanal minas cheese. Food Res Int 2018; 107: 406-13.
[http://dx.doi.org/10.1016/j.foodres.2018.02.009] [PMID: 29580501]
[27]
Gotteland M, Cires MJ, Carvallo C. Vega N, Ramirez MA,Morales P, et al. Probiotic screening and safety evaluation of Lactobacillus strains from plants, artisanal goat cheese, human stools, and breast milk. J Med Food 2014; 17(4): 487-95.
[http://dx.doi.org/10.1089/jmf.2013.0030] [PMID: 24433075]
[28]
Baruzzi F, Poltronieri P, Quero GM, Morea M, Morelli L. An in vitro protocol for direct isolation of potential probiotic lactobacilli from raw bovine milk and traditional fermented milks. Appl Microbiol Biotechnol 2011; 90(1): 331-42.
[http://dx.doi.org/10.1007/s00253-011-3133-6] [PMID: 21318359]
[29]
Liu Q, Ni X, Wang Q, Peng Z, Niu L, Xie M, et al. Investigation of lactic acid bacteria isolated from giant panda feces for potential probiotics invitro. [online]. Probiotics Antimicrob Proteins 2019; 15;11(1): 85-91.
[30]
Fraqueza MJ. Antibiotic resistance of lactic acid bacteria isolated from dry-fermented sausages. Int J Food Microbiol 2015; 212: 76-88.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2015.04.035] [PMID: 26002560]
[31]
Santos KMO, Vieira ADSV, Buriti FCA, Nascimento J, Silva de Melo ME, Bruno LM, et al. Artisanal Coalho cheeses as source of beneficial Lactobacillus plantarum and Lactobacillus rhamnosus strains. Dairy Sci Technol 2015; 95(2): 209-30.
[http://dx.doi.org/10.1007/s13594-014-0201-6]
[32]
Kumar M, Ghosh M, Ganguli A. Mitogenic response and probiotic characteristics of lactic acid bacteria isolated from indigenously pickled vegetables and fermented beverages. World J Microbiol Biotechnol 2012; 28(2): 703-11.
[http://dx.doi.org/10.1007/s11274-011-0866-4] [PMID: 22806866]
[33]
Ramos CL, Thorsen L, Schwan RF, Jespersen L. Strain-specific probiotics properties of Lactobacillus fermentum, Lactobacillus plantarum and Lactobacillus brevis isolates from Brazilian food products. Food Microbiol 2013; 36: 22-9.
[34]
Solieri L, Bianchi A, Mottolese G, Lemmetti F, Giudici P. Tailoring the probiotic potential of non-starter Lactobacillus strains from ripened Parmigiano Reggiano cheese by in vitro screening and principal component analysis. Food Microbiol 2014; 38: 240-9.
[http://dx.doi.org/10.1016/j.fm.2013.10.003] [PMID: 24290648]
[35]
Shori AB. Influence of food matrix on the viability of probiotic bac- teria: A review based on dairy and non-dairy beverages. Food Biosci 2016; 13: 1-8.
[http://dx.doi.org/10.1016/j.fbio.2015.11.001]
[36]
Cruz AG, Antunes AEC, Sousa ALOP, Faria JAF, Saad SMI. Ice-cream as a probiotic food carrier. Food Res Int 2009; 42: 1233-9.
[http://dx.doi.org/10.1016/j.foodres.2009.03.020]
[37]
Ferraz JL, Cruz AG, Cadena RS. Freitas MQ, Pinto UM, Carvalho CC, set al. Sensory acceptance and survival of probiotic bacteria in ice cream produced with different overrun levels. J Food Sci 2012; 77(1): S24-8.
[http://dx.doi.org/10.1111/j.1750-3841.2011.02508.x] [PMID: 22260128]
[38]
Senanayake SA, Fernando S, Bamunuarachchi A, Arsekularatne M. Application of Lactobacillus acidophilus (LA 5) strain in fruit-based ice cream. Food Sci Nutr 2013; 1(6): 428-31.
[http://dx.doi.org/10.1002/fsn3.66] [PMID: 24804052]
[39]
Hampe CS, Roth CL. Probiotic strains and mechanistic insights for the treatment of type 2 diabetes. Endocrine 2017; 58(2): 207-27.
[http://dx.doi.org/10.1007/s12020-017-1433-z] [PMID: 29052181]
[40]
Tripathi MK, Giri SK. Probiotic functional foods: Survival of probiotics during processing and storage. J Funct Foods 2014; 9: 225-41.
[http://dx.doi.org/10.1016/j.jff.2014.04.030]
[41]
Shah NP, Ding WK, Fallourd MJ, Leyer G. Improving the stability of probiotic bacteria in model fruit juices using vitamins and antioxidants. J Food Sci 2010; 75(5): M278-82.
[http://dx.doi.org/10.1111/j.1750-3841.2010.01628.x] [PMID: 20629884]
[42]
Petyaev IM, Bashmakov YK. Cocobiota: Implications for Human Health. J Nutr Metab 2016; 20167906927
[http://dx.doi.org/10.1155/2016/7906927] [PMID: 27144019]
[43]
Eskes A, Guarda D, Garcia L, Garcia R. Is genetic variation for sensory traits of cocoa pulp related to fine flavour cocoa traits?Ingenic newsletters 2007; 11: 22-8.
[44]
Tzounis X, Rodriguez-Mateos A, Vulevic J, Gibson GR, Kwik-Uribe C, Spencer JP. Prebiotic evaluation of cocoa-derived flavanols in healthy humans by using a randomized, controlled, double-blind, crossover intervention study. Am J Clin Nutr 2011; 93(1): 62-72.
[http://dx.doi.org/10.3945/ajcn.110.000075] [PMID: 21068351]
[45]
Yao MF, Wu J, Li B, Xiao H, McClements DJ, Li LJ. Microencapsulation of Lactobacillus salivarious Li01 for enhanced storage viability and targeted delivery to gut microbiota. Food Hydrocoll 2017; 72: 228-36.
[http://dx.doi.org/10.1016/j.foodhyd.2017.05.033]