Safety, functional properties and technological performance in whey-based media of probiotic candidates from human breast milk

International Microbiology - Tập 22 - Trang 265-277 - 2018
María Florencia Zacarías1, Ana Binetti1, Wilhelm Bockelmann2, Jorge Reinheimer1, Knut Heller2, Gabriel Vinderola1
1Instituto de Lactología Industrial (INLAIN, UNL-CONICET), Facultad de Ingeniería Química, Universidad Nacional del Litoral, Santa Fe, Argentina
2Department of Microbiology and Biotechnology, Max Rubner-Institut, Federal Research Institute of Nutrition and Food, Kiel, Germany

Tóm tắt

We aimed at isolating and characterising microorganisms present in human breast milk with probiotic potential. In an 8-week postpartum sampling period, two strains of bifidobacteria (Bifidobacterium longum LM7a and Bifidobacterium dentium LM8a’) and four strains of lactobacilli were isolated, all during the first 4-week postpartum. B. longum LM7a and B. dentium LM8a’, together with four strains previously isolated from breast milk (Bifidobacterium lactis INL1, INL2, INL4 and INL5), were considered for further studies. Susceptibility of the strains to tetracycline, erythromycin, clindamycin, streptomycin, vancomycin and chloramphenicol was evaluated and the isolates exhibited, in general, the same properties as previously reported for bifidobacteria. All isolates showed low hydrophobicity and B. lactis and B. longum strains had satisfactory resistance to gastric digestion and bile shock, but not to pancreatin. B. lactis INL1, B. longum LM7a and B. dentium LM8a’ were selected for some comparative technological studies. In particular, B. lactis INL1 displayed technological potential, with satisfactory growth in cheese whey-based media in biofermentor and resistance to freeze-drying, accelerated storage conditions and simulated gastric digestion.

Tài liệu tham khảo

Ammor MS, Flórez AB, van Hoek AH, de Los Reyes-Gavilán CG, Aarts HJ, Margolles A, Mayo B (2008) Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria. J Mol Microbiol Biotechnol 14:6–15 Arboleya S, Ruas-Madiedo P, Margolles A, Solís G, Salminen S, de Los Reyes-Gavilán CG, Gueimonde M (2011) Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol 149(1):28–36 Balciunas EM, Al Arni S, Converti A, Leblanc JG, Oliveira RP dS (2016) Production of bacteriocin-like inhibitory substances (BLIS) by Bifidobacterium lactis using whey as a substrate. Int J Dairy Technol 69:236–242 Binetti A, Suárez V, Tailliez P, Reinheimer J (2007) Characterization of spontaneous phage-resistant variants of Streptococcus thermophilus by randomly amplified polymorphic DNA analysis and identification of phage-resistance mechanisms. Int Dairy J 17:1115–1122 Boix-Amorós A, Collado MC, Mira A (2016) Relationship between milk microbiota, bacterial load, macronutrients, and human cells during lactation. Front Microbiol 7:492 Burns P, Lafferriere L, Vinderola G, Reinheimer J (2014) Influence of dairy practices on the capacity of probiotic bacteria to overcome simulated gastric digestion. Int J Dairy Technol 67:448–457 Burns P, Alard J, Hrdy J, Boutillier D, Páez R, Reinheimer J, Pot B, Vinderola G, Grangette C (2017) Spray-drying effect on the protective capacity of the breast milk-derived Bifidobacterium lactis INL1 on acute and chronic colitis in mice. Sci Rep 7:43211 Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 6(3):544–551 Cabrera-Rubio R, Mira-Pascual L, Mira A, Collado MC (2015) Impact of mode of delivery on the milk microbiota composition of healthy women. J Dev Orig Health Dis 7(1):54–60 Cardamone L, Quiberoni A, Mercanti DJ, Fornasari ME, Reinheimer JA, Guglielmotti DM (2011) Adventitious dairy Leuconostoc strains with interesting technological and biological properties useful for adjunct starters. Dairy Sci Technol 91(4):457–470 Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, Gibbs P (2004) Relevant factors for the preparation of freeze-dried lactic acid bacteria. Int Dairy J 14:835–847 Chassard C, de Wouters T, Lacroix C (2014) Probiotics tailored to the infant: a window of opportunity. Curr Opin Biotechnol 26:141–147 Choi K, Ryu J, Kwak H (2010) Spray-dried conjugated linoleic acid encapsulated with maillard reaction products of whey proteins and maltodextrin. Food Sci Biotechnol 19:957–965 Corre C, Madec MN, Boyaval P (1992) Production of concentrated Bifidobacterium bifidum. J Chem Technol Biotechnol 53:189–194 Deepika G, Green RJ, Frazier RA, Charalampopoulos D (2009) Effect of growth time on the surface and adhesion properties of Lactobacillus rhamnosus GG. J Appl Microbiol 107(4):1230–1240 Deepika G, Karunakaran E, Hurley CR, Biggs CA, Charalampopoulos D (2012) Influence of fermentation conditions on the surface properties and adhesion of Lactobacillus rhamnosus GG. Microb Cell Factories 11:116 Doleyres Y, Lacroix C (2005) Technologies with free and immobilised cells for probiotic bifidobacteria production and protection. Int Dairy J 15:973–988 Edwards U, Rogall T, Blockerl H, Emde M, Bottger E (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853 European Food Safety Authority (EFSA) Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2008) Technical guidance - update of the criteria used in the assessment of bacterial resistance to antibiotics of human or veterinary importance. EFSA J 732:1–15 European Food Safety Authority (EFSA) Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA J 10:2740 FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group report. Available at ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. Accessed 17/09/2017 FDA (2005) Additional correspondence, GRAS notice n° GRN 000049. Available at http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm154391.htm. Accessed 17/09/2017 FDA (2013) GRAS notice n° GRN 000445. Available at http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm352951.htm. Accessed 17/09/2017 Fernández L, Langa S, Martín V, Maldonado A, Jiménez E, Martín R, Rodríguez JM (2013) The human milk microbiota: origin and potential roles in health and disease. Pharmacol Res 69(1):1–10 Giraffa G, Andrighetto G, Antonello C, Gatti M, Lazzi C, Marcazzan G, Lombardi A, Neviani E (2004) Genotypic and phenotypic diversity of Lactobacillus delbrueckii subsp. lactis strains of dairy origin. Int J Food Microbiol 91:129–139 Gotteland M, Cruchet S, Brunser O (2011) Functional food in child nutrition. In: Functional food product development. Wiley, Chicester, pp 440–458 Grimm V, Westermann C, Riedel CU (2014) Bifidobacteria-host interactions: an update on colonisation factors. Biomed Res Int 2014:1–10. https://doi.org/10.1155/2014/960826 Grönlund MM, Gueimonde M, Laitinen K, Kociubinski G, Grönroos T, Salminen S, Isolauri E (2007) Maternal breast-milk and intestinal bifidobacteria guide the compositional development of the Bifidobacterium microbiota in infants at risk of allergic disease. Clin Exp Allergy 37(12):1764–1772 Grześkowiak Ł, Isolauri E, Salminen S, Gueimonde M (2011) Manufacturing process influences properties of probiotic bacteria. Br J Nutr 105(6):887–894 Gueimonde M, Sánchez B (2012) Enhancing probiotic stability in industrial processes. Microb Ecol Health Dis 23. https://doi.org/10.3402/mehd.v23i0.18562 Gueimonde M, Laitinen K, Salminen S, Isolauri E (2007) Breast milk: a source of bifidobacteria for infant gut development and maturation? Neonatol 92(1):64–66 Gueimonde M, Flórez AB, van Hoek AH, Stuer-Lauridsen B, Strøman P, de los Reyes-Gavilán CG, Margolles A (2010) Genetic basis of tetracycline resistance in Bifidobacterium animalis subsp. lactis. Appl Environ Microbiol 76:3364–3369 Han YR, Youn SY, Ji GE, Park MS (2014) Production of α- and β-galactosidases from Bifidobacterium longum subsp. longum RD47. J Microbiol Biotechnol 24(5):675–682 Heller KJ (2001) Probiotic bacteria in fermented foods: product characteristics and starter organisms. Am J Clin Nutr 73:374S–379S Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514 Hsu CA, Yu RC, Lee SL, Chou CC (2007) Cultural condition affecting the growth and production of beta-galactosidase by Bifidobacterium longum CCRC 15708 in a jar fermenter. Int J Food Microbiol 116(1):186–189 Huys G, D'Haene K, Cnockaert M, Tosi L, Danielsen M, Flórez AB, Mättö J, Axelsson L, Korhonen J, Mayrhofer S, Egervärn M, Giacomini M, Vandamme P (2010) Intra- and interlaboratory performances of two commercial antimicrobial susceptibility testing methods for bifidobacteria and nonenterococcal lactic acid bacteria. Antimicrob Agents Chemother 54(6):2567–2574 Jankovic I, Sybesma W, Phothirath P, Ananta E, Mercenier A (2010) Application of probiotics in food products—challenges and new approaches. Curr Opin Biotechnol 21:175–181 Jeurink PV, van Bergenhenegouwen J, Jiménez E, Knippels LM, Fernández L, Garssen J, Knol J, Rodríguez JM, Martín R (2013) Human milk: a source of more life than we imagine. Benefic Microbes 4:17–30 Kozak K, Charbonneau D, Sanozky-Dawes R, Klaenhammer T (2015) Characterization of bacterial isolates from the microbiota of mothers’ breast milk and their infants. Gut Microbes 6(6):341–351 Kushiro A, Chervaux C, Cools-Portier S, Perony A, Legrain-Raspaud S, Obis D, Onoue M, van de Moer A (2009) Antimicrobial susceptibility testing of lactic acid bacteria and bifidobacteria by broth microdilution method and Etest. Int J Food Microbiol 132(1):54–58 Lavari L, Páez R, Cuatrin A, Reinheimer J, Vinderola G (2014) Use of cheese whey for biomass production and spray drying of probiotic lactobacilli. J Dairy Res 81(3):267–274 Le Huërou-Luron I, Blat S, Boudry G (2010) Breast- v. formula-feeding: impacts on the digestive tract and immediate and long-term health effects. Nutr Res Rev 23:3–36 Lee YK, Puong KY (2002) Competition for adhesion between probiotics and human gastrointestinal pathogens in the presence of carbohydrate. Br J Nutr 88(1):S101–S108 Mainville I, Arcand Y, Farnworth ER (2005) A dynamic model that simulates the human upper gastrointestinal tract for the study of probiotics. Int J Food Microbiol 99(3):287–296 Maldonado J, Cañabate F, Sempere L, Vela F, Sánchez AR, Narbona E, López-Huertas E, Geerlings A, Valero AD, Olivares M, Lara-Villoslada F (2012) Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J Pediatr Gastroenterol Nutr 54(4):55–61 Martín R, Olivares M, Marín ML, Fernández L, Xaus J, Rodríguez JM (2005) Probiotic potential of 3 Lactobacilli strains isolated from breast milk. J Hum Lact 21(1):8–17 Martín R, Jiménez E, Heilig H, Fernández L, Marín ML, Zoetendal EG, Rodríguez JM (2009) Isolation of bifidobacteria from breast milk and assessment of the bifidobacterial population by PCR-denaturing gradient gel electrophoresis and quantitative real-time PCR. Appl Environ Microbiol 75:965–969 Masco L, Crockaert C, Van Hoorde K, Swings J, Huys G (2007) In vitro assessment of the gastrointestinal transit tolerance of taxonomic reference strains from human origin and probiotic product isolates of Bifidobacterium. J Dairy Sci 90:3572–3578 Matsumoto M, Ohishi H, Benno Y (2004) H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93:109–113 Mättö J, Malinen E, Suihko ML, Alander M, Palva A, Saarela M (2004) Genetic heterogeneity and functional properties of intestinal bifidobacteria. J Appl Microbiol 97(3):459–470 Mättö J, Alakomi HL, Vaari A, Virkajarvi I, Saarela M (2006) Influence of processing conditions on Bifidobacterium animalis subsp. lactis functionality with a special focus on acid tolerance and factors affecting it. Int Dairy J 16:1029–1037 Mättö J, van Hoek AH, Domig KJ, Saarela M, Flórez AB, Brockmann E, Amtmann E, Mayo B, Aarts HJ, Danielsen M (2007) Susceptibility of human and probiotic Bifidobacterium spp. to selected antibiotics as determined by the Etest method. Int Dairy J 17:1123–1131 Mayrhofer S, Domig KJ, Mair C, Zitz U, Huys G, Kneifel W (2008) Comparison of broth microdilution, Etest, and agar disk diffusion methods for antimicrobial susceptibility testing of Lactobacillus acidophilus group members. Appl Environ Microbiol 74(12):3745–3748 Pannaraj PS, Li F, Cerini C, Bender JM, Yang S, Rollie A, Adisetiyo H, Zabih S, Lincez PJ, Bittinger K, Bailey A, Bushman FD, Sleasman JW, Aldrovandi GM (2017) Association between breast milk bacterial communities and establishment and development of the infant gut microbiome. JAMA Pediatr 171(7):647–654 Pérez Guerra N, Fajardo Bernárdez P, Méndez J, Cachaldor P, Pastrana Castro L (2007) Production of four potentially probiotic lactic acid bacteria and their evaluation as feed additives for weaned piglets. Anim Feed Sci Technol 134:89–107 Reis NA, Saraiva MA, Duarte EA, de Carvalho EA, Vieira BB, Evangelista-Barreto NS (2016) Probiotic properties of lactic acid bacteria isolated from human milk. J Appl Microbiol 121(3):811–820 Romano-Keeler J, Weitkamp JH (2015) Maternal influences on fetal microbial colonization and immune development. Pediatr Res 77(1–2):189–195 Saad N, Delattre C, Urdaci M, Schmitter JM, Bressollier P (2013) An overview of the last advances in probiotic and prebiotic field. LWT Food Sci Technol 50:1–16 Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York Santos M, Tymczyszyn E, Golowczyc M, Mobili P, Gomez-Zavaglia A (2016) Probiotic cell cultivation. In: Foerst P, Santivarangkna C (eds) Advances in probiotic technology. CRC Press, Boca Ratón, pp 45–76 Shakirova L, Grube M, Gavare M, Auzina L, Zikmanis P (2013) Lactobacillus acidophilus La5 and Bifidobacterium lactis Bb12 cell surface hydrophobicity and survival of the cells under adverse environmental conditions. J Ind Microbiol Biotechnol 40(1):85–93 Souza TC, Silva AM, Drews JRP, Gomes DA, Vinderola CG, Nicoli JR (2013) In vitro evaluation of Bifidobacterium strains of human origin for potential use in probiotic functional foods. Benefic Microbes 4(2):179–186 Toscano M, De Grandi R, Peroni DG, Grossi E, Facchin V, Comberiati P, Drago L (2017) Impact of delivery mode on the colostrum microbiota composition. BMC Microbiol 17(1):205 Tosi L, Berruti G, Danielsen M, Wind A, Huys G, Morelli L (2007) Susceptibility of Streptococcus thermophilus to antibiotics. Antonie Van Leeuwenhoek 92(1):21–28 Vael C, Desager K (2009) The importance of the development of the intestinal microbiota in infancy. Curr Opin Pediatr 21(6):794–800 Ventura M, Turroni F, Zomer A, Foroni E, Giubellini V, Bottacini F, Canchaya C, Claesson MJ, He F, Mantzourani M, Mulas L, Ferrarini A, Gao B, Delledonne M, Henrissat B, Coutinho P, Oggioni M, Gupta RS, Zhang Z, Beighton D, Fitzgerald GF, O'Toole PW, van Sinderen D (2009) The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5(12):e1000785 Vinderola CG, Reinheimer JA (2003) Lactic acid starter and probiotic bacteria: a comparative in vitro study of probiotic characteristics and biological barrier resistance. Food Res Int 36(9–10):895–904 Vinderola CG, Medici M, Perdigón G (2004) Relationships between interaction sites in the gut, hydrophobicity, mucosal immunomodulating capacities and cell-wall protein profiles in lactic acid bacteria. J Appl Microbiol 96(2):230–243 Vinderola G, Zacarías MF, Bockelmann W, Neve H, Reinheimer J, Heller KJ (2012) Preservation of functionality of Bifidobacterium animalis subsp. lactis INL1 after incorporation of freeze-dried cells into different food matrices. Food Microbiol 30(1):274–280 Williams JE, Carrothers JM, Lackey KA, Beatty NF, York MA, Brooker SL, Shafii B, Price WJ, Settles ML, McGuire MA, McGuire MK (2017) Human milk microbial community structure is relatively stable and related to variations in macronutrient and micronutrient intakes in healthy lactating women. J Nutr 147(9):1739–1748 Young SL, Sarda X, Rosenberg M (1993) Microencapsulating properties of whey proteins. Combination of whey proteins with carbohydrates. J Dairy Sci 76:2878–2885 Zacarías MF, Binetti A, Laco M, Reinheimer J, Vinderola G (2011) Preliminary technological and probiotic characterization of bifidobacteria isolated from breast milk for use in dairy products. Int Dairy J 21:548–555 Zacarías MF, Reinheimer J, Forzani L, Grangette C, Vinderola G (2014) Mortality and translocation assay to study the protective capacity of Bifidobacterium lactis INL1 against Salmonella Typhimurium infection in mice. Benefic Microbes 5(4):427–436 Zacarías MF, Souza TC, Zaburlín N, Carmona Cara D, Reinheimer J, Nicoli J, Vinderola G (2017) Influence of technological treatments on the functionality of Bifidobacterium lactis INL1, a breast milk-derived probiotic. J Food Sci 82(10):2462–2470