The Effect of Royal Jelly on Growth and Short-Chain Fatty Acid Production of Probiotic Bacteria and Activity of Bacterial Procarcinogenic Enzymes in Rat Faeces

Open access

The present study was done to evaluate the effect of three different royal jelly samples on the kinetic growth of two isolates of lactic bacteria; Lactobacillusacidophilus and Bifidobacterium bifidum. The results showed that the addition of royal jelly supported and improved the growth of L. acidophilus and B. bifidum. The highest count of L. acidophilus was 9.01 (log10 cfu/mL) when 2% (w/v) of the royal jelly sample 3 was added to milk. The highest count of B. bifidum was 9.07 (log10 cfu/mL) when 5% (w/v) of the royal jelly sample 1 was added to milk. Based on the obtained results, royal jelly showed the capability of prebiotic activity and increasing the activity of L. acidophilus and B. bifidum. Royal jelly promotes SCFAs productions which are believed to have an antitumor effect. The results showed the presence of signifi cant synbiotic effect of fermented milk and royal jelly on the intestinal microflora. This effect is translated by the reduction in the faecal enzyme activities of β-glucuronidase, arylsulphatase, and β-gluconsidase which are involved in colon carcinogenesis.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Awaisheh S. In vitro studies of the effect of fermented dairy products containing probiotics and neutraceuticals on different characteristics of normal flora. Ph.D. 2003 Thesis University of Jordan Amman Jordan.

  • 2. Bernardeau M. Vernoux J.P. Henri-Dubernet S. Guéguen M. Safety assessment of dairy microorganisms: The Lactobacillus genus. Int. J. Food Microbiol. 2008 126 SI 278-285.

  • 3. Bezkorovainy A. Probiotics: determinants of survival and growth in the gut. Am. J. Clin. Nutr. 2001 73 S399-S405.

  • 4. Bincoletto C. Eberlin S. Figueiredo C.A.V. Luengo M.B. Queiroz M.L. Effects produced by royal jelly on haematopoiesis: relation with host resistance against Ehrlich ascites tumour challenge. Int. Immunopharmacol. 2005 5 679-688.

  • 5. Burns A.J. Rowland I.R. Anti-carcinogenicity of probiotics and prebiotics. Curr. Issues Intest. Microbiol. 2000 1 13- -24.

  • 6. Djouzi Z. Andrieux C. Degivry M.-C. Bouley C. Szylit O. The association of yogurt starters with Lactobacillus casei DN 114.001 in fermented milk alters the composition and metabolism of intestinal microfl ora in germ-free rats and in human fl ora-associated rats. J. Nutr. 1997 127 2260-2266.

  • 7. El-Nekeety A.A. El-Kholy W. Abbas N.F. Ebaid A. Amra H.A. Abdel-Wahhab M.A. Effi cacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon 2007 50 256-269.

  • 8. Goldin B.R. Gorbach S.L. The effect of milk and lactobacilli feeding on human intestinal bacteria enzyme activity. Am. J. Clin. Nutr. 1984 39 756-761.

  • 9. Guarner F. Malagelada J.R. Gut fl ora in health and disease. Lancet 2003 361 512-519.

  • 10. Haddadin M.S.Y. Nazer I. Sara’ J.R. Robinson R.K. Effect of honey on the growth and metabolism of two bacterial species of intestinal origin. Pakistan J. Nutr. 2007 6 693-697.

  • 11. Hinnebusch B.F. Meng S.F. Wu J.T. Archer S.Y. Hodin R.A. The effects of short-chain fatty acids on human colon cancer cell phenotype are associated with histone hyperacetylation. J. Nutr. 2002 132 1012-1017.

  • 12. Hyang M.A. Shin Y.P. Do K.L. Jung R.K. Min K.C. Si W.L. Hyung T.L. Kyung J.K. Nam J.H. Antiobesity and lipid-lowering effects of Bifi dobacterium spp. in high fat diet-induced obese rats. Lipids Health Dis. 2011 10 116.

  • 13. Inoue S. Koya-Miyata S. Ushio S. Iwaki K. Ikeda M. Kurimoto M. Royal jelly prolongs the life span of C3H/HeJ mice: correlation with reduced DNA damage. Exp. Gerontol. 2003 38 965-969.

  • 14. Kailasapathy K. Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifi dobacterium spp. Immunol. Cell Biol. 2000 78 80-88.

  • 15. Kamakura M. Mitani N. Fukuda T. Fukushima M. Antifatigue effect of fresh royal jelly in mice. J. Nutr. Sci. Vitaminol. 2001 47 394-401.

  • 16. Kohno K. Okamoto I. Sano O. Arai N. Iwaki K. Ikeda M. Kurimoto M. Royal jelly inhibits the production of proinfl ammatory cytokines by activated macrophages. Biosci. Biotechnol. Biochem. 2004 68 138-145.

  • 17. Leblank A.D. Perdigon G. Reduction of β-glucuronidase and nitroreductase activity by yoghurt in a murine colon cancer model. Biocell 2005 29 15-24.

  • 18. Lichtenthaler R. Marx F. Total oxidant scavenging capacities of common European fruit and vegetable juices. J. Agric. Food Chem. 2005 53 103-110.

  • 19. Liong M.T. Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in vivo evidence. Int. J. Mol. Sci. 2008 9 854-863.

  • 20. Marsili R.T. Ostapenkoo H. Simmons R.E. Green D.E. High performance liquid chromatography determination of organic acids in dairy products. J. Food Sci. 1981 46 52-57.

  • 21. Marteau P. Pochart P. Flourie B. Pellier P. Santos L. Desjeux J.F. Rambaud J.C. Effect of chronic ingestion of a fermented dairy product containing Lactobacillus acidophilus and Bifi dobacteriumbifi dum on metabolic activities of the colonic fl ora in humans. Am. J. Clin. Nutr. 1990 52 685-688.

  • 22. Matsui T. Yukiyoshi A. Doi S. Sugimoto H. Yamada H. Matsumoto K. Gastrointestinal enzyme production of bioactive peptides from royal jelly protein and their antihypertensive ability in SHR. J. Nutr. Biochem. 2002 13 80-86.

  • 23. Nagai T. Inoue R. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food Chem. 2004 84 181-186.

  • 24. Nyman M. Fermentation and bulking capacity of indigestible carbohydrates: the case of inulin and oligofructose. Br. J. Nutr. 2002 87 S163-S168.

  • 25. Okamoto I. Taniguchi Y. Kunikita T. Kohno K. Iwaki K. Ikeda M. Kurimoto M. Major royal jelly protein 3 modulates immune responses in vitro and in vivo. Life Sci. 2003 73 2029-2045.

  • 26. Pan X.D. Chen F.Q. Wu T.X. Tang H.G. Zhao Z.Y. Prebiotic oligosaccharides change the concentrations of short-chain fatty acids and the microbial population of mouse bowel. J. Zhejiang Univ. Sci. B 2009a 10 258-263.

  • 27. Pan X.D. Chen F.Q. Wu T.X. Tang H.G. Zhao Z.Y. The acid bile tolerance and antimicrobial property of Lactobacillus acidophilus NIT. Food Contr. 2009b 20 598-602.

  • 28. Perez-Conesa D. Lopez G. Ros G. Fermentation capabilities of bifi dobacteria using nondigestible oligosaccharides and their viability as probiotics in commercial powder infant formula. J. Food Sci. 2005 70 M279-M285.

  • 29. Pool-Zobel B.L. Neudecker C. Domizlaff I. Schillinger S. Ji U. Rumney C. Moretti M. Vilarini I. Scassellati-Sforzolini R. Rowland I. Lactobacillus- and Bifi dobacterium-mediated antigenotoxicity in the colon of rats. Nutr. Cancer 1996 26 365-380.

  • 30. Roberfroid M.B. Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 2000 71 1682-1687.

  • 31. Roberfroid M.B. Prebiotics: preferential substrates for specifi c germs? Am. J. Clin. Nutr. 2001 73 407S-415S.

  • 32. Rossi M. Corradini C. Amaretti A. Nicolini M. Pompei A. Zanoni S. Matteuzzi D. Fermentation of fructooligosaccharides and inulin by bifi dobacteria: a comparative study of pure and fecal cultures. Appl. Environ. Microbiol. 2005 71 6150-6158.

  • 33. Saarela M. Mättö J. Mattila-Sandholm T. Safety aspects of Lactobacillus and Bifi dobacterium species originating from human oro-gastrointestinal tract or from probiotic products. Microb. Ecol. Health Dis. 2002a 14 234-241.

  • 34. Saarela M. Lahteenmaki L. Crittenden R. Salminen S. Mattila- Sandholm T. Gut bacteria and health foods - the European perspective. Int. J. Food Microbiol. 2002b 78 SI 99-117.

  • 35. Sanz M.L. Polemis N. Morales V. Coezo N. Drakoularakou A. Gibson G.R. Rastal R.A. In vitro investigation into the potential prebiotic activity of honey oligosaccharides. J. Agric. Food Chem. 2005 53 2914-2921.

  • 36. Sauerwald N. Polster J. Bengsch E. Niessen L. Vogel R.F. Combined antibacterial and antifungal properties of water-soluble fraction of royal jelly. Adv. Food Sci. 1998 20 46-52.

  • 37. Saxelin M. Tynkkynen S. Mattila-Sandholm T. De Vos W.M. Probiotic and other functional microbes: from markets to mechanisms. Curr. Opin. Biotechnol. 2005 16 204-211.

  • 38. Shanahan F. Probiotics and infl ammatory bowel disease: from fads and fantasy to facts and future. Br. J. Nutr. 2002 88 (Suppl. 1) S5-S9.

  • 39. Stocker A. Schramel P. Kettrup A. Bengsch E. Trace and mineral elements in royal jelly and homeostatic effects. J. Trace Elem. Med. Biol. 2005 19 183-189.

  • 40. Topping D.L. Short chain fatty acids produced by intestinal bacteria. Asia Pac. J. Clin. Nutr. 1996 5 15-19.

  • 41. Upadhyay N. Moudgal V. Probiotics: A Review. JCOM 2012 19 76-84.

  • 42. Verschuren P.M. Functional foods: scientifi c and global perspectives. Br. J. Nutr. 2002 88 S125-S130.

  • 43. Watanabe K. Shinmoto H. Kobori M. Tsushida T. Shimohara K. Kanaeda J. Yonekura M. Growth stimulation with honey royal jelly DIII protein of human lymphocytic cell lines in a serum- free medium. Biotechnol. Tech. 1996 10 959-962.

  • 44. Watanabe K. Shinmoto H. Kobori M. Tsushida T. Shimohara K. Kanaeda J. Yonekura M. Stimulation of cell growth in the U-937 human myeloid cell line by honey royal jelly protein. Cytotechnology 1998 26 23-27.

  • 45. Wollowski I. Rechkemmer G. Pool-Zobel B.L. Protective role of probiotics and prebiotics in colon cancer Am. J. Clin. Nutr. 2001 73(suppl) 451S-5S.

  • 46. Yang X.Y. Yang D.S. Wei-Zhang Wang J.M. Li C.Y. Hui Y. Lei K.F. Chen X.F. Shen N.H. Jin L.Q. Wang J.G. 10-Hydroxy- 2-decenoic acid from Royal jelly: A potential medicine for RA. J. Ethnopharmacol. 2010 128 314-321.

  • 47. Zimmermann A. Liver regeneration: the emergence of new pathways. Med. Sci. Monit. 2002 8 3 RA 53-63.

Search
Journal information
Impact Factor


IMPACT FACTOR 2017: 1.697
5-year IMPACT FACTOR: 1.760



CiteScore 2018: 1.92

SCImago Journal Rank (SJR) 2018: 0.621
Source Normalized Impact per Paper (SNIP) 2018: 0.908

Cited By
Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 373 104 3
PDF Downloads 166 64 2