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Fungal Probiotics: Opportunity, Challenge, and Prospects

  • Abhijit Banik
  • Suman Kumar Halder
  • Chandradipa Ghosh
  • Keshab Chandra Mondal
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

The discovery of several fungal strains as probiotics is expanding a new era in the probiotic family. Because of their unique cellular architecture and better survivability in the harsh environment of the gastrointestinal tract, fungi are significant probiotic candidates. As the exact mechanism of action, efficacy, and dosage level are not fully understood, the implementation of new fungal strains in a therapeutic approach is not completely validated. Among the fungal strains isolated as probiotic candidates, Saccharomyces boulardii var. cerevisiae is the most promising commercialized probiotic yeast: it exerts several health beneficial effects in both normal and adverse physiological states of the host body. Researchers around the world have tried to evaluate the efficacy of newly isolated probiotic fungi for better bioavailability as well as safety issues. This chapter mainly focuses on newly isolated probiotic fungal stains, their mechanism of action, their health benefits, and also their efficacy in the treatment of various diarrheal, skin, and vaginal complications. Some future prospects regarding safety issues and better industrial application are also covered in this chapter.

Keywords

Fungal probiotic Health beneficial effects Mechanism of action Saccharomyces boulardii 

Notes

Acknowledgments

The first author is grateful to the Department of Physiology, Midnapore College (Autonomous), West Bengal, India.

References

  1. Agheyisi R (2014) The probiotics market: ingredients, supplements, foods. Report code: FOD035C. BCC Research, WellesleyGoogle Scholar
  2. Amorim JC, Piccoli RH, Duarte WF (2018) Probiotic potential of yeasts isolated from pineapple and their use in the elaboration of potentially functional fermented beverages. Food Res Int 107:518–527CrossRefGoogle Scholar
  3. Badia R, Zanello G, Chevaleyre C, Lizardo R, Meurens F, Martínez P, Salmon H (2012) Effect of Saccharomyces cerevisiae var. boulardii and β-galactomannan oligosaccharide on porcine intestinal epithelial and dendritic cells challenged in vitro with Escherichia coli F4 (K88). J Vet Res 43(1):4CrossRefGoogle Scholar
  4. Besirbellioglu BA, Ulcay A, Can M, Erdem H, Tanyuksel M, Avci IY, Araz E, Pahsa A (2006) Saccharomyces boulardii and infection due to Giardia lamblia. Scand J Infect Dis 38:479–481CrossRefGoogle Scholar
  5. Bisson JF, Hidalgo S, Rozan P, Messaoudi M (2010) Preventive effects of different probiotic formulations on travelers’ diarrhea model in wistar rats. Dig Dis Sci 55(4):911–919CrossRefGoogle Scholar
  6. Bontempo V, Di Giancamillo A, Savoini G, Dell’Orto V, Domeneghini C (2006) Live yeast dietary supplementation acts upon intestinal morpho-functional aspects and growth in weanling piglets. Anim Feed Sci Technol 129:224–236CrossRefGoogle Scholar
  7. Butler AR, White JH, Stark MJ (1991) Analysis of the response of Saccharomyces cerevisiae cells to Kluyveromyces lactis toxin. Microbiology 137(7):1749–1757Google Scholar
  8. Buts JP, De Keyser N (2006) Effects of Saccharomyces boulardii on intestinal mucosa. Dig Dis Sci 51(8):1485–1492CrossRefGoogle Scholar
  9. Buts JP, Bernasconi P, Vaerman JP, Dive C (1990) Stimulation of secretory IgA and secretory component of immunoglobulins in small intestine of rats treated with Saccharomyces boulardii. Dig Dis Sci 35(2):251–256CrossRefGoogle Scholar
  10. Buts JP, de Keyser N, Marandi S (1999) Saccharomyces boulardii upgrades cellular adaptation after proximal enterectomy in rats. Gut 45:89–96CrossRefGoogle Scholar
  11. Chen X, Kokkotou EG, Mustafa N, Bhaskar KR, Sougioultzis S, O’Brien M, Pothoulakis C, Kelly C (2006) Saccharomyces boulardii inhibits ERK1/2 mitogen-activated protein kinase activation both in vitro and in vivo, and protects against Clostridium difficile toxin A-induced enteritis. J Biol Chem 281(34):24449–22454CrossRefGoogle Scholar
  12. Chen X, Fruehauf J, Goldsmith JD, Xu H, Katchar KK, Koon HW, Zhao D, Kokkotou EG, Pothoulakis C, Kelly CP (2009) Saccharomyces boulardii inhibits EGF receptor signaling and intestinal tumor growth in Apcmin mice. Gastroenterol 137(3):914–923CrossRefGoogle Scholar
  13. Chen X, Yang G, Song JH, Xu H, Li D, Goldsmith J, Zeng H, Parsons-Wingerter PA, Reinecker HC, Kelly CP (2013) Probiotic yeast inhibits VEGFR signaling and angiogenesis in intestinal inflammation. PLoS One 8(5):64227CrossRefGoogle Scholar
  14. Cho YJ, Kim DH, Jeong D, Seo KH, Jeong HS, Lee HG, Kim H (2018) Characterization of yeasts isolated from kefir as a probiotic and its synergic interaction with the wine byproduct grape seed flour/extract. LWT 90:535–539CrossRefGoogle Scholar
  15. Cremonini F, Di Caro S, Covino M, Armuzzi A, Gabrielli M, Santarelli Nista EC, Cammarota G, Gasbarrini G, Gasbarrini A (2002) Effect of different probiotic preparations on anti-Helicobacter pylori therapy-related side effects: a parallel group, triple blind, placebo-controlled study. Am J Gastroenterol 97:2744–2749CrossRefGoogle Scholar
  16. Czerucka D, Piche T, Rampal P (2007) Yeast as probiotics–Saccharomyces boulardii. Aliment Pharmacol Ther 26(6):767–778CrossRefGoogle Scholar
  17. Dahan S, Dalmasso G, Imbert V, Peyron JF, Rampal P, Czerucka D (2003) Saccharomyces boulardii interferes with enterohemorrhagic Escherichia coli-induced signaling pathways in T84 cells. Infect Immun 71(2):766–773CrossRefGoogle Scholar
  18. Dube HC (2013) An introduction to fungi. Scientific Publishers.Google Scholar
  19. El-Baz AF, El-Enshasy HA, Shetaia YM, Mahrous H, Othman NZ, Yousef AE (2018) Semi-industrial scale production of a new yeast with probiotic traits, Cryptococcus sp. YMHS, isolated from the Red Sea. Probiotics Antimicrob Proteins 10(1):77–88CrossRefGoogle Scholar
  20. FAO/WHO, (2006) Probiotics in food: health and nutritional properties and guidelines for evaluation, FAO Food and Nutrition Paper no. 85, FAO/WHO, Rome, ItalyGoogle Scholar
  21. Fadda ME, Mossa V, Deplano M, Pisano MB, Cosentino S (2017) In vitro screening of Kluyveromyces strains isolated from Fiore Sardo cheese for potential use as probiotics. LWT-Food Sci Technol 75:100–106CrossRefGoogle Scholar
  22. Falagas ME, Betsi GI, Athanasiou S (2006) Probiotics for prevention of recurrent vulvovaginal candidiasis: a review. J Antimicrob Chemother 58(2):266–272CrossRefGoogle Scholar
  23. Fernández M, Hudson JA, Korpela R, de los Reyes-Gavilán CG (2015) Impact on human health of microorganisms present in fermented dairy products: an overview. Bio Med Res Int 2015:412714.  https://doi.org/10.1155/2015/412714CrossRefGoogle Scholar
  24. Foligné B, Dewulf J, Vandekerckove P, Pignède G, Pot B (2010) Probiotic yeasts: anti-inflammatory potential of various non-pathogenic strains in experimental colitis in mice. World J Gastroenterol 16(17):2134–2145CrossRefGoogle Scholar
  25. Fuller R (1992) History and development of probiotics. In: Probiotics. Springer, Dordrecht, pp 1–8CrossRefGoogle Scholar
  26. Ghoneum M, Matsuura M, Braga M, Gollapudi S (2008) S. cerevisiae induces apoptosis in human metastatic breast cancer cells by altering intracellular Ca2+ and the ratio of Bax and Bcl-2. Int J Oncol 33(3):533–539PubMedGoogle Scholar
  27. Girard P, Pansart Y, Gillardin JM (2005) Inducible nitric oxide synthase involvement in the mechanism of action of Saccharomyces boulardii in castor oil-induced diarrhoea in rats. Nitric Oxide 13(3):163–169CrossRefGoogle Scholar
  28. Gotteland M, Poliak L, Cruchet S, Brunser O (2005) Effect of regular ingestion of Saccharomyces boulardii plus inulin or Lactobacillus acidophilus LB in children colonized by Helicobacter pylori. Acta Paediatr 94:1747–1751CrossRefGoogle Scholar
  29. Guslandi M, Mezzi G, Sorghi M, Testoni PA (2000) Saccharomyces boulardii in maintenance treatment of Crohn’s disease. Dig Dis Sci 45:1462–1464CrossRefGoogle Scholar
  30. Guslandi M, Giollo P, Testoni PA (2003) A pilot trial of Saccharomyces boulardii in ulcerative colitis. Eur J Gastroenterol Hepatol 15:697–698CrossRefGoogle Scholar
  31. Hjortmo SB, Hellström AM, Andlid TA (2008) Production of folates by yeasts in Tanzanian fermented togwa. FEMS Yeast Res 8(5):781–787CrossRefGoogle Scholar
  32. Holzapfel WH (2002) Appropriate starter culture technologies for small-scale fermentation in developing countries. Int J Food Microbiol 75(3):197–212CrossRefGoogle Scholar
  33. Hurduc V, Plesca D, Dragomir D, Sajin M, Vandenplas Y (2009) A randomized, open trial evaluating the effect of Saccharomyces boulardii on the eradication rate of Helicobacter pylori infection in children. Acta Paediatr 98:127–131CrossRefGoogle Scholar
  34. Jadán-Piedra C, Baquedano M, Puig S, Vélez D, Devesa V (2017) Use of Saccharomyces cerevisiae to reduce the bioaccessibility of mercury from food. J Agric Food Chem 65(13):2876–2882CrossRefGoogle Scholar
  35. Katz JA (2006) Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile diarrhea. J Clin Gastroenterol 40:249–255CrossRefGoogle Scholar
  36. Kelesidis T, Pothoulakis C (2012) Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therap Adv Gastroenterol 2:111–125CrossRefGoogle Scholar
  37. Kogani G, Pajtinka M, Babincova M, Miadokova E, Rauko P, Slamenova D, Korolenko TA (2008) Yeast cell wall polysaccharides as antioxidants and antimutagens: can they fight cancer? Minireview. Neoplasma 55(5):387Google Scholar
  38. Kollaritsch H, Holst H, Grobara P, Wiedermann G (1993) Prevention of traveler’s diarrhea with Saccharomyces boulardii. Results of a placebo controlled double-blind study. Fortschr Med 111(9):152–156PubMedGoogle Scholar
  39. Kotowska M, Albrecht P, Szajewska H (2005) Saccharomyces boulardii in the prevention of antibiotic-associated diarrhoea in children: a randomized double-blind placebo-controlled trial. Aliment Pharmacol Ther 21:583–590CrossRefGoogle Scholar
  40. Križková L, Ďuračková Z, Šandula J, Sasinková V, Krajčovič J (2001) Antioxidative and antimutagenic activity of yeast cell wall mannans in vitro. Mutat Res Genet Toxicol Environ Mutagen 497(1):213–222CrossRefGoogle Scholar
  41. Kroemer G, Reed JC (2000) Mitochondrial control of cell death. Nat Med 6(5):513–519CrossRefGoogle Scholar
  42. Kumar V, Yadav AN, Verema P, Sangwan P, Abhishake S, Singh B (2017) β-Propeller phytases: diversity, catalytic attributes, current developments and potential biotechnological applications. Int J Biol Macromolec 98:595–609CrossRefGoogle Scholar
  43. Kumura H, Tanoue Y, Tsukahara M, Tanaka T, Shimazaki K (2004) Screening of dairy yeast strains for probiotic applications. J Dairy Sci 87(12):4050–4056CrossRefGoogle Scholar
  44. Lee SK, Kim HJ, Chi SG, Jang JY, Nam KD, Kim NH, Joo KR, Dong SH, Kim BH, Chang YW, Lee JI (2005) Saccharomyces boulardii activates expression of peroxisome proliferator-activated receptor-gamma in HT-29 cells. Korean J Gastroenterol 45(5):328–334PubMedGoogle Scholar
  45. Lessard M, Dupuis M, Gagnon N, Nadeau E, Matte JJ, Goulet J, Fairbrother JM (2009) Administration of Pediococcus acidilactici or Saccharomyces cerevisiae boulardii modulates development of porcine mucosal immunity and reduces intestinal bacterial translocation after Escherichia coli challenge. J An Sci 87(3): 922–934Google Scholar
  46. Lim MH, Lee OH, Chin JE, Ko HM, Kim IC, Lee HB, Bai S (2008) Simultaneous degradation of phytic acid and starch by an industrial strain of Saccharomyces cerevisiae producing phytase and α-amylase. Biotechnol Lett 30(12):2125–2130CrossRefGoogle Scholar
  47. Lipke PN, Ovalle R (1998) Cell wall architecture in yeast: new structure and new challenges. Int J Bacteriol 180(15):3735–3740Google Scholar
  48. Maccaferri S, Klinder A, Brigidi P, Cavina P, Costabile A (2012) Potential probiotic Kluyveromyces marxianus B0399 modulates the immune response in Caco-2 cells and peripheral blood mononuclear cells and impacts the human gut microbiota in an in vitro colonic model system. Appl Environ Microbiol 78(4):956–964CrossRefGoogle Scholar
  49. Mansour-Ghanaei F, Dehbashi N, Yazdanparast K, Shafaghi A (2003) Efficacy of Saccharomyces boulardii with antibiotics in acute amoebiasis. World J Gastroenterol 9:1832–1833CrossRefGoogle Scholar
  50. 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):8–17CrossRefGoogle Scholar
  51. Martins FS, Nardi RM, Arantes RM, Rosa CA, Neves MJ, Nicoli JR (2005) Screening of yeasts as probiotic based on capacities to colonize the gastrointestinal tract and to protect against enteropathogen challenge in mice. J Gen Appl Microbiol 51(2):83–92CrossRefGoogle Scholar
  52. Maupas JL, Champemont P, Delforge M (1983) Treatment of irritable bowel syndrome. Double blind trial of Saccharomyces boulardii. Med Chir Dig 12(12):77–79Google Scholar
  53. McFarland LV (2007) Meta-analysis of probiotics for the prevention of traveler’s diarrhea. Travel Med Infect Dis 5:97–105CrossRefGoogle Scholar
  54. McFarland LV (2010) Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol 16(18):2202–2022CrossRefGoogle Scholar
  55. Mumy KL, Chen X, Kelly CP, McCormick BA (2008) Saccharomyces boulardii interferes with Shigella pathogenesis by post invasion signaling events. Am J Physiol Gastrointest Liver Physiol 294(3):599–609CrossRefGoogle Scholar
  56. Nurmi JT, Puolakkainen PA, Rautonen NE (2005) Bifidobacterium lactis sp. 420 up-regulates cyclooxygenase (Cox)-1 and down-regulates Cox-2 gene expression in a Caco-2 cell culture model. Nutr Cancer 51(1):83–92CrossRefGoogle Scholar
  57. Ochangco HS, Gamero A, Smith IM, Christensen JE, Jespersen L, Arneborg N (2016) In vitro investigation of Debaryomyces hansenii strains for potential probiotic properties. World J Microbiol Biotechnol 32(9):141CrossRefGoogle Scholar
  58. Olstorpe M, Schnürer J, Passoth V (2009) Screening of yeast strains for phytase activity. FEMS Yeast Res 9(3):478–488CrossRefGoogle Scholar
  59. Ooi CY, Dilley AV, Day AS (2009) Saccharomyces boulardii in a child with recurrent Clostridium difficile. Pediatr Int 51(1):156–158CrossRefGoogle Scholar
  60. Ozkan TB, Sahin E, Erdemir G, Budak F (2007) Effect of Saccharomyces boulardii in children with acute gastroenteritis and its relationship to the immune response. J Int Med Res 35(2):201–212CrossRefGoogle Scholar
  61. Padayachee M, Visser J, Viljoen E, Musekiwa A, Blaauw R (2018) Efficacy and safety of Saccharomyces boulardii in the treatment of acute gastroenteritis in the paediatric population: a systematic review. South Afr J Clin Nutr 4(1):1–12Google Scholar
  62. Péteri Z, Téren J, Vágvölgyi C, Varga J (2007) Ochratoxin degradation and adsorption caused by astaxanthin-producing yeasts. Food Microbiol 24(3):205–210CrossRefGoogle Scholar
  63. Plein K, Hotz J (1993) Therapeutic effects of Saccharomyces boulardii on mild residual symptoms in a stable phase of Crohns disease with special respect to chronic diarrhea – a pilot-study. Z Gastroenterol 31:129–134PubMedGoogle Scholar
  64. Puppala KR, Kumar VR, Khire J, Dharne M (2018) Dephytinizing and probiotic potentials of Saccharomyces cerevisiae (NCIM 3662) strain for amelioration of nutritional quality of functional foods. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9394-y
  65. Qamar A, Aboudola S, Warny M, Michetti P, Pothoulakis C, LaMont JT, Kelly CP (2001) Saccharomyces boulardii stimulates intestinal immunoglobulin a immune response to Clostridium difficile toxin a in mice. Infect Immun 69(4):2762–2765CrossRefGoogle Scholar
  66. Ragon M, Aumelas A, Chemardin P, Galvez S, Moulin G, Boze H (2008) Complete hydrolysis of myo-inositol hexakisphosphate by a novel phytase from Debaryomyces castellii CBS 2923. Appl Microbiol Biotechnol 78(1):47–53CrossRefGoogle Scholar
  67. Rima H, Steve L, Ismail F (2012) Antimicrobial and probiotic properties of yeasts: from fundamental to novel applications. Front Microbiol 3:421Google Scholar
  68. Rodrigues ACP, Cara DC, Fretez SHGG, Cunha FQ, Vieira EC, Nicoli JR, Vieira LQ (2000) Saccharomyces boulardii stimulates sIgA production and the phagocytic system of gnotobiotic mice. J Appl Microbiol 89(3):404–414CrossRefGoogle Scholar
  69. Sabater-Vilar M, Malekinejad H, Selman MHJ, Van der Doelen MAM, Fink-Gremmels J (2007) In vitro assessment of adsorbents aiming to prevent deoxynivalenol and zearalenone mycotoxicoses. Mycopathologia 163(2):81–90CrossRefGoogle Scholar
  70. Saber A, Alipour B, Faghfoori Z, Khosroushahi AY (2017) Secretion metabolites of dairy Kluyveromyces marxianus AS41 isolated as probiotic, induces apoptosis in different human cancer cell lines and exhibit anti-pathogenic effects. J Funct Foods 34:408–421CrossRefGoogle Scholar
  71. Sanders JW, Tribble DR (2001) Diarrhea in the returned traveler. Curr Gastroenterol Rep 3:304–314CrossRefGoogle Scholar
  72. Sartor RB (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterol 126(6):1620–1633CrossRefGoogle Scholar
  73. Sharma D, Saharan BS (2018) Microbial cell factories. CRC Press, Boca RatonCrossRefGoogle Scholar
  74. Silva JFMD, Peluzio JM, Prado G, Madeira JEGC, Silva MO, de Morais PB, Nicoli JR (2015) Use of probiotics to control aflatoxin production in peanut grains. Sci World J 2015:959138., 8 pages.  https://doi.org/10.1155/2015/959138CrossRefGoogle Scholar
  75. Silva-Aciares FR, Carvajal PO, Mejias CA, Riquelme CE (2011) Use of macroalgae supplemented with probiotics in the Haliotis rufescens (Swainson, 1822) culture in Northern Chile. Aquac Res 42(7):953–961Google Scholar
  76. Smith IM, Christensen JE, Arneborg N, Jespersen L (2014) Yeast modulation of human dendritic cell cytokine secretion: an in vitro study. PLoS One 9(5):e96595CrossRefGoogle Scholar
  77. Smith IM, Baker A, Christensen JE, Boekhout T, Frøkiær H, Arneborg N, Jespersen L (2016) Kluyveromyces marxianus and Saccharomyces boulardii induce distinct levels of dendritic cell cytokine secretion and significantly different T cell responses in vitro. PLoS One 11(11):e0167410CrossRefGoogle Scholar
  78. Srinivas B, Rani GS, Kumar BK, Chandrasekhar B, Krishna KV, Devi TA, Bhima B (2017) Evaluating the probiotic and therapeutic potentials of Saccharomyces cerevisiae strain (OBS2) isolated from fermented nectar of toddy palm. AMB Express 7(1):2CrossRefGoogle Scholar
  79. Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R, Mulligan ME, Garcia RJ, Brandmarker S, Bowen K, Borjal D, Elmer GW (2000) The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis 31:1012–1017CrossRefGoogle Scholar
  80. Swidsinski A, Loening-Baucke V, Verstraelen H, Osowska S, Doerffel Y (2008) Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology 135(2):568–579CrossRefGoogle Scholar
  81. Tiago FCP, Porto BAA, Ribeiro NS, Moreira LMC, Arantes RME, Vieira AT, Teixeira MM, Generoso SV, Nascimento VN, Martins FS, Nicoli JR (2015) Effect of Saccharomyces cerevisiae strain UFMG A-905 in experimental model of inflammatory bowel disease. Benef Microbes 6(6):807–815CrossRefGoogle Scholar
  82. Vilela EG, Ferrari MDD, Torres HOD, Pinto AG, Aguirre ACC, Martins FP, Goulart EMA, Da Cunha AS (2008) Influence of Saccharomyces boulardii on the intestinal permeability of patients with Crohn’s disease in remission. Scand J Gastroenterol 43:842–848CrossRefGoogle Scholar
  83. Weber G, Adamczyk A, Freytag S (1989) Treatment of acne with a yeast preparation. Fortschr Med 26:563–566Google Scholar
  84. Weiler F, Schmitt MJ (2003) Zygocin, a secreted antifungal toxin of the yeast Zygosaccharomyces bailii, and its effect on sensitive fungal cells. FEMS Yeast Res 3(1):69–76PubMedGoogle Scholar
  85. Witthuhn RC, Schoeman T, Britz TJ (2005) Characterisation of the microbial population at different stages of Kefir production and Kefir grain mass cultivation. Int Dairy J 15(4):383–389Google Scholar
  86. Yadav AN, Kumar R, Kumar S, Kumar V, Sugitha T, Singh B, Chauhan VS, Dhaliwal HS, Saxena AK (2017a) Beneficial microbiomes: biodiversity and potential biotechnological applications for sustainable agriculture and human health. J Appl Biol Biotechnol 5:1–13CrossRefGoogle Scholar
  87. Yadav AN, Verma P, Kumar R, Kumar S, Kumar V, Kumar K, Dhaliwal HS (2017b) Probiotic microbes: biodiversity, mechanisms of action and potential role in human health. In: Proceedings of National Conference on Advances in Food Science and Technology, pp 33–34Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Abhijit Banik
    • 1
  • Suman Kumar Halder
    • 2
  • Chandradipa Ghosh
    • 1
  • Keshab Chandra Mondal
    • 2
  1. 1.Department of Human Physiology with Community HealthVidyasagar UniversityMidnaporeIndia
  2. 2.Department of MicrobiologyVidyasagar UniversityMidnaporeIndia

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