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Characterization of edible swiftlet’s nest as a prebiotic ingredient using a simulated colon model

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Abstract

Purpose

Edible bird’s nest (EBN) has been considered as one of the nutritious foods and was also claimed to aid in digestion problems. Potential prebiotic of the EBN for gut health by the presence of glycan within the complex structure of the EBN glycoprotein to date has not been reported. The gut health can contribute to the overall consumers’ health in the improvement of the gut beneficial bacterial growth. In this study, the potential prebiotic of the EBN was conducted using a simulation of in vitro human colon model system.

Methods

The EBN-extracted glycan and EBN glycoprotein (crude sample) were digested using in vitro oral, gastric and duodenal model system. Prebiotic activities of the undigested EBN glycan and EBN glycopeptide compounds were studied with the fructooligosaccharide as a positive control, using inoculum of 10% (w/v) faecal bacteria in the in vitro fermentation system.

Result

The fermentation of EBN glycan and EBN glycopeptide had shown significant increases of the gut beneficial bacteria and was comparable with fructooligosaccharide fermentation, with each sample presented different profiles of bacterial growth. The fermentation of EBN glycan and EBN glycopeptide demonstrated an increase in the total short-chain fatty acid production, particularly acetate, propionate and butyrate.

Conclusion

These findings suggested that the EBN can be functioned as a natural prebiotic upon consumption, thus providing a potential as prebiotic ingredients.

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References

  • Aguirre M, Eck A, Koenen ME, Savelkoul H, Budding AE, Venema K (2016) Diet drives quick changes in the metabolic activity and composition of human gut microbiota in a validated in vitro gut model. Res Microbiol 167:114–125

    CAS  PubMed  Google Scholar 

  • Altonsy MO, Andrews SC, Tuohy KM (2010) Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: mediation by the mitochondrial pathway. Int J Food Microbiol 137:190–203

    PubMed  Google Scholar 

  • Angelidaki I, Ahring BK (1995) Isomerization of n-andi-butyrate in anaerobic methanogenic systems. Antonie Van Leeuwenhoek 68:285–291

    CAS  PubMed  Google Scholar 

  • Bailey MT, Cryan JF (2017) The microbiome as a key regulator of brain, behavior and immunity: commentary on the 2017 named series. Brain Behav Immun 66:18–22

    PubMed  Google Scholar 

  • Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. J Appl Environ Microbiol 72:3593–3599

    CAS  Google Scholar 

  • Bottari B, Quartieri A, Prandi B, Raimondi S, Leonardi A, Rossi M, Ulrici A, Gatti M, Sforza S, Nocetti M, Amaretti A (2017) Characterization of the peptide fraction from digested Parmigiano Reggiano cheese and its effect on growth of lactobacilli and bifidobacteria. Int J Food Microbiol 255:32–41

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Carbonaro M, Maselli P, Nucara A (2012) Relationship between digestibility and secondary structure of raw and thermally treated legume proteins: a Fourier transform infrared (FT-IR) spectroscopic study. Amino Acids 43:911–921

    CAS  PubMed  Google Scholar 

  • Cardelle-Cobas A, Corzo N, Olano A, Peláez C, Requena T, Ávila M (2011) Galactooligosaccharides derived from lactose and lactulose: influence of structure on Lactobacillus, Streptococcus and Bifidobacterium growth. Int J Food Microbiol 149:81–87

    CAS  PubMed  Google Scholar 

  • Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ (2015) Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis 26:26191

    PubMed  Google Scholar 

  • Church FC, Swaisgood HE, Porter DH, Catignani GL (1983) Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins. J Dairy Sci 66:1219–1227

    CAS  Google Scholar 

  • Deutz NEP, Ten Have GAM, Soeters PB, Moughan PJ (1995) Increased intestinal amino-acid retention from the addition of carbohydrates to a meal. Clin Nutr 14:354–364

    CAS  PubMed  Google Scholar 

  • Dhingra D, Michael M, Rajput H, Patil RT (2012) Dietary fibre in foods: a review. J Food Sci Technol 49:255–266

    CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64: 3336–3345

  • Gardner ML (1988) Gastrointestinal absorption of intact proteins. Annu Rev Nutr 8:329–350

    CAS  PubMed  Google Scholar 

  • Haghani A, Mehrbod P, Safi N, Aminuddin NA, Bahadoran A, Omar AR, Ideris A (2016) In vitro and in vivo mecanism of immunomodulatory and antiviral activity of Edible Bird's Nest (EBN) against influenza A virus (IAV) infection. J Ethnopharmacol 185: 327–340

    PubMed  Google Scholar 

  • Hayisama-Ae W, Kantachote D, Bhongsuwan D, Nokkaew U, Chaiyasut C (2014) A potential synbiotic beverage from fermented red seaweed (Gracilariafisheri) using Lactobacillus plantarum DW12. Int Food Res J 21:1789–1796

    CAS  Google Scholar 

  • Harmsen HJ, Elfferich P, Schut F, Welling GW (1999) A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microbiol Ecology in Health and Disease 11: 3–12

  • Harmsen HJ, Wildeboer-Veloo AC, Grijpstra J, Knol J, Degener JE, Welling GW (2000) Development of 16S rRNA-based probes for Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 66: 4523–4527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hernández-Hernández O, Muthaiyan A, Moreno FJ, Montilla A, Sanz ML, Ricke SC (2012) Effect of prebiotic carbohydrates on the growth and tolerance of Lactobacillus. Food Microbiol 30:355–361

    PubMed  Google Scholar 

  • Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HJ (2003) Oligonucleotide probes that detect quantitatively significant groups of butyrateproducing bacteria in human feces. Appl Environ Microbiol 69: 4320–4324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G Jr, Goh YJ, Hamaker B, Martens EC, Mills DA, Rastal RA, Vaughan E (2016) Prebiotics: why definitions matter. Curr Opin Biotechnol 37:1–7

    CAS  PubMed  Google Scholar 

  • Jiménez-Colmenero F, Cofrades S, Herrero AM, Ruiz-Capillas C (2018) Implications of domestic food practices for the presence of bioactive components in meats with special reference to meat-based functional foods. Crit Rev Food Sci Nutr 58(14):2334–2345

    PubMed  Google Scholar 

  • Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10:323

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphius GR, Wilkinson MH, Welling GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61: 3069–3075

  • Larsen JM (2017) The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology 151:363–374

    CAS  PubMed  PubMed Central  Google Scholar 

  • LeBlanc JG, Chain F, Martín R, Bermúdez-Humarán LG, Courau S, Langella P (2017) Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microbial Cell Fact 16:79

    Google Scholar 

  • Lie A, Pedersen LH (2016) Analysis of human milk oligosaccharides using high-performance anion-exchange chromatography with pulsed amperometric detection. In: 11th Danish Conf Biotechnol Mol Biol, Denmark.

  • Liu F, Li P, Chen M, Luo Y, Prabhakar M, Zheng H, He Y, Qi Q, Long H, Zhang Y, Sheng H (2017) Fructooligosaccharide (FOS) and galactooligosaccharide (GOS) increase bifidobacterium but reduce butyrate producing bacteria with adverse glycemic metabolism in healthy young population. Scientific Reports 7: 11789

  • Lopetuso LR, Scaldaferri F, Petito V, Gasbarrini A (2013) Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog 5:23

    PubMed  PubMed Central  Google Scholar 

  • Louis P, Young P, Holtrop G, Flint HJ (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA: acetate CoA-transferase gene. Environ Microbiol 12:304–314

    CAS  PubMed  Google Scholar 

  • Luo D, Li Y, Xu B, Ren G, Li P, Li X, Han S, Liu J (2017) Effects of inulin with different degree of polymerization on gelatinization and retrogradation of wheat starch. Food Chem 229:35–43

    CAS  PubMed  Google Scholar 

  • Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142: 1097–1106

    CAS  PubMed  Google Scholar 

  • Matthies C, Schink B (1992) Reciprocal isomerization of butyrate and isobutyrate by the strictly anaerobic bacterium strain WoG13 and methanogenic isobutyrate degradation by a defined triculture. Appl Environ Microbiol 58:1435–1439

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minekus M, Alminger M, Alvito P, Ballance S, Bohn T, Bourlieu C, Carriere F, Boutrou R, Corredig M, Dupont D, Dufour C (2014) A standardised static in vitro digestion method suitable for food–an international consensus. Food Funct 5:1113–1124

    CAS  PubMed  Google Scholar 

  • Morrison DJ, Preston T (2016) Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:189–200

    PubMed  PubMed Central  Google Scholar 

  • Ndeh D, Gilbert HJ (2018) Biochemistry of complex glycan depolymerisation by the human gut microbiota. FEMS Microbiol Rev 42:146–164

    CAS  PubMed  Google Scholar 

  • Rios-Covian D, Salazar N, Gueimonde M, de los Reyes-Gavilan CG (2017) Shaping the metabolism of intestinal Bacteroides population through diet to improve human health. Front Microbiol 8:376

    PubMed  PubMed Central  Google Scholar 

  • Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L (2016) Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 7:979

    PubMed  PubMed Central  Google Scholar 

  • Saqib AAN, Whitney PJ (2011) Differential behaviour of the dinitrosalicylic acid (DNS) reagent towards mono-and di-saccharide sugars. Biomass Bioenergy 35:4748–4750

    CAS  Google Scholar 

  • Sarbini SR, Kolida S, Naeye T, Einerhand A, Brison Y, Remaud-Simeon M, Monsan P, Gibson GR,Rastall RA (2011) In vitro fermentation of linear and α-1, 2 branched dextrans by the human faecal microbiota. Appl Environ Microbiol 77: 5307–5315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawicki CM, Livingston KA, Obin M, Roberts SB, Chung M, McKeown NM (2017) Dietary fiber and the human gut microbiota: Application of evidence mapping methodology. Nutrients 9:125

    PubMed Central  Google Scholar 

  • Tailford LE, Crost EH, Kavanaugh D, Juge N (2015) Mucin glycan foraging in the human gut microbiome. Front Genet 6:81

    PubMed  PubMed Central  Google Scholar 

  • Takaishi H, Matsuki T, Nakazawa A, Takada T, Kado S, Asahara T, Kamada N, Sakuraba A, Yajima T, Higuchi H, Inoue N (2008) Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int J Med Microbiol 298:463–472

    CAS  PubMed  Google Scholar 

  • Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A, Sánchez B, Bidossi A, Ferrarini A, Giubellini V, Delledonne M (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc National Acad Sci 107:19514–19519

    CAS  Google Scholar 

  • Turroni F, Ventura M, Buttó LF, Duranti S, O’Toole PW, Motherway MOC, van Sinderen D (2014) Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71:183–203

    CAS  PubMed  Google Scholar 

  • Utomo B, Rosyidi D, Radiati LE, Puspaningsih NNT, Proborini WD (2014) Protein characterization of extracted water from three kinds of edible bird nest using SDS-PAGE CBB staining and SDS-PAGE glycoprotein staining and LC-MS/MS analyses. IOSR J Agr Vet Sci 7:33–38

    Google Scholar 

  • Van der Meulen R, Makras L, Verbrugghe K, Adriany T, De Vuyst L (2006) In vitro kinetic analysis of oligofructose consumption by Bacteroides and Bifidobacterium spp, indicates different degradation mechanisms. Appl Environ Microbiol 72:1006–1012

    PubMed  PubMed Central  Google Scholar 

  • Walker WA (2017) The importance of appropriate initial bacterial colonization of the intestine in newborn, child, and adult health. Pediatr Res 82:387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walker AW, Duncan SH, Leitch ECM, Child MW, Flint HJ (2005) pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl Environ Microbiol 71:3692–3700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Whitman WB, Bowen TL, Boone DR (2006) The methanogenic bacteria. Prokaryotes 3:165–207

    Google Scholar 

  • Wieruszeski JM, Michalski JC, Montreuil J, Strecker G, Peter-Katalinic J, Egge H, Van Halbeek H, Mutsaers JH, Vliegenthart JF (1987) Structure of the monosialyl oligosaccharides derived from salivary gland mucin glycoproteins of the Chinese swiftlet (genus Collocalia). J Biol Chem 262:6650–6657

    CAS  PubMed  Google Scholar 

  • Xian XM, Hou Y, Lin JR, Huang S, Lai XP, Chen JN (2010) Study on degradation of protein of the edible birds’ nest (Aerodramus) in vitro. J Chin Med Mat 33:1760–1763

    CAS  Google Scholar 

  • Yagi H, Yasukawa N, Yu SY, Guo CT, Takahashi N, Takahashi T, Bukawa W, Suzuki T, Khoo KH, Suzuki Y, Kato K (2008) The expression of sialylated high-antennary N-glycans in edible bird’s nest. Carbohydr Res 343:1373–1377

    CAS  PubMed  Google Scholar 

  • You Y, Cao Y, Guo S, Xu J, Li Z, Wang J, Xue C (2015) Purification and identification of α 2–3 linked sialoglycoprotein and α 2–6 linked sialoglycoprotein in edible bird’s nest. Eur Food Res Technol 240:389–397

    CAS  Google Scholar 

  • Yu ZT, Chen C, Kling DE, Liu B, McCoy JM, Merighi M, Heidtman M, Newburg DS (2012) The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23:169–177

    PubMed  PubMed Central  Google Scholar 

  • Zhu L, Qin S, Zhai S, Gao Y, Li L (2017) Inulin with different degrees of polymerization modulates composition of intestinal microbiota in mice. FEMS Microbiol Lett 364

  • Zimmer J, Lange B, Frick JS, Sauer H, Zimmermann K, Schwiertz A et al (2012) A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur J Clin Nutr 66:53–60

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank the participating students from Universiti Putra Malaysia Campus Bintulu for their voluntary participation.

Funding

This work was supported by CoE-Swiftlet Project under Grant (6371400-10301-(PN3): UPM/ST-2016-013: UKM).

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Correspondence to Abdul Salam Babji.

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This article does contain studies with human participants performed by the authors.

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No ethical approval was obtained because this study did not involve laboratory animals and only involved non-invasive procedures. Informed consent was obtained from all individual participants included in the study.

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Daud, N., Sarbini, S.R., Babji, A.S. et al. Characterization of edible swiftlet’s nest as a prebiotic ingredient using a simulated colon model. Ann Microbiol 69, 1235–1246 (2019). https://doi.org/10.1007/s13213-019-01507-1

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  • DOI: https://doi.org/10.1007/s13213-019-01507-1

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