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References

  1. Connolly ML, Lovegrove JA, Tuohy KM. 2010. Konjac glucomannan hydrolysate beneficially modulates bacterial composition and activity within the faecal microbiota. J. Funct. Foods 2: 219-224.
    CrossRef
  2. Duangkaewmanee S, Petsom A. 2011. Synergistic and antagonistic effects on oxidation stability of antioxidants in a synthetic ester based oil. Tribol. Int. 44: 266-271.
    CrossRef
  3. Ferrario C, Taverniti V , Milani C, Fiore W, Laureati M, De Noni I, et al. 2014. Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillus paracasei DG varies among healthy adults. J. Nutr. 144: 17871796.
    Pubmed CrossRef
  4. Kao TH, Chen BH. 2006. Functional components in soybean cake and their effects on antioxidant activity. J. Agric. Food Chem. 54: 7544-7555.
    Pubmed CrossRef
  5. Kimmel SA, Roberts RF. 1998. Development of a growth medium suitable for exopolysaccharide production by Lactobacillus delbrueckii ssp. bulgaricus RR. Int. J. Food Microbiol. 40: 87-92.
    CrossRef
  6. Li M, Xu Y, Yang W, Li J, Xu X, Zhang X , et al. 2011. In vitro synergistic antioxidant activities of solvent-extracted fractions from Astragalus membranaceus and Glycyrrhiza uralensis. LWT Food Sci. Technol. 44: 1745-1751.
    CrossRef
  7. Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. 2014. An in vitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe 27: 50-55.
    Pubmed CrossRef
  8. Ma C, Feng M, Zhai X, Hu M, You L, Luo W, Zhao M. 2013. Optimization for the extraction of polysaccharides from Ganoderma lucidum and their antioxidant and antiproliferative activities. J. Taiwan Inst. Chem. E 44: 886-894.
    CrossRef
  9. Madhukumar MS, Muralikrishna G. 2010. Structural characterisation and determination of prebiotic activity of purified xylo-oligosaccharides obtained from Bengal gram husk (Cicer arietinum L.) and wheat bran (Triticum aestivum). Food Chem. 118: 215-223.
    CrossRef
  10. Makras L, Triantafyllou V , Messaoudi D F, Adriany T , Zoumpopoulou G, Tsakalidou E, et al. 2006. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res. Microbiol. 157: 241-247.
    Pubmed CrossRef
  11. Manisseri C, Gudipati M. 2010. Bioactive xylo-oligosaccharides from wheat bran soluble polysaccharides. LWT Food Sci. Technol. 43: 421-430.
    CrossRef
  12. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, et al. 2010. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302: 1-18.
    CrossRef
  13. Moura P, Cabanas S, Lourenco P, Girio F, Dias MCL, Esteves MP. 2008. In vitro fermentation of selected xylooligosaccharides by piglet intestinal microbiota. LWT Food Sci. Technol. 41: 1952-1961.
    CrossRef
  14. Moura P, Marques S, Alves J, Freire JPB, Cunha LF, Esteves MP. 2007. Effect of xylo-oligosaccharides from corn cobs autohydrolysis on the intestinal microbiota of piglets after weaning. Lives Sci. 108: 244-248.
    CrossRef
  15. Moure A, Gullón P, Domínguez H, Parajó JC. 2006. Advances in the manufacture, purification and applications of xylo-oligosaccharides as food additives and nutraceuticals. Process Biochem. 41: 1913-1923.
    CrossRef
  16. Muthu R, Thangavel P, Selvaraj N, Ramalingam R, Vaiyapuri M. 2013. Synergistic and individual effects of umbelliferone with 5-flurouracil on the status of lipid peroxidation and antioxidant defense against 1,2-dimethylhydrazine induced rat colon carcinogenesis. Biomed. Prev. Nutr. 3: 74-82.
    CrossRef
  17. Niki E. 2010. Assessment of antioxidant capacity in vitro and in vivo. Free Radical Biol. Med. 49: 503-515.
    Pubmed CrossRef
  18. Pan X , Wu T, Zhang L , Cai L , Song Z. 2 009. I nfluence o f oligosaccharides on the growth and tolerance capacity of lactobacilli to simulated stress environment. Lett. Appl. Microbiol. 48: 362-367.
    Pubmed CrossRef
  19. Ren T, Lu F, Zhang Y , Cheng Z , Xu M. 2010. I ntake of a high fat diet alters intestinal flora in rats. World J. Digest. 8: 2694-2697.
  20. 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.
    CrossRef
  21. Samanta K , Senani S, Kolte AP, Sridhar M, Sampath KT, Jayapal N, Devi A. 2009. Production and in vitro evaluationof xylooligosaccharides generated from corn cobs. Food Bioprod. Process. 90: 466-474.
    CrossRef
  22. Scheppach W, Luehrs H, Menzel T. 2001. Beneficial health effects of low-digestible carbohydrate consumption. Br. J. Nutr. 85: 23-30.
    CrossRef
  23. Schneider SM, Pipau FG, Anty R, Linde EGM, Geerling BJP, Knol J, et al. 2006. Effects of total enteral nutrition supplemented with a multi-fibre mix on faecal short-chain fatty acids and microbiota. Clin. Nutr. 25: 82-90.
    Pubmed CrossRef
  24. Shanks D, Maharik NA, Malmström J, Engman L, Eriksson P, Stenberg B, Reitberger T. 2003. Improved antioxidant formulations for polymeric materials – synergistic protective effects in combinations of organotellurium compounds with conventional phenolic antioxidants or thiols. Polym. Degrad. Stab. 81: 261-271.
    CrossRef
  25. Vrese M, Schrezenmeir JS. 2008. Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 111: 1-66.
    Pubmed CrossRef
  26. Vulevic J, Rastall RA, Gibson GR. 2004. Developing a quantitative approach for determining the in vitro prebiotic potential of dietary oligosaccharides. FEMS Microbiol. Lett. 236: 153-159.
    Pubmed CrossRef
  27. Wang S, Meckling KA, Marcone MF, Kakuda Y, Proulx A, Tsao R. 2012. In vitro antioxidant synergism and antagonism between food extracts can lead to similar activities in H2O2induced cell death, caspase-3 and MMP-2 activities in H9c2 cells. J. Sci. Food Agric. 92: 2983-2993.
    Pubmed CrossRef
  28. Ye C, Hu W, Dai D. 2011. Extraction of polysaccharides and the antioxidant activity from the seeds of Plantago asiatica L. Int. J. Biol. Macromol. 49: 466-470.
    Pubmed CrossRef
  29. Yuan X, Wang J, Yao H. 2004. Antioxidant activity of feruloylated oligosaccharides from wheat bran. Food Chem. 90: 759-764.
    CrossRef
  30. Zampa A, Silvi S, Fabiani R, Morozzi G, Orpianesi C, Cresci A. 2004. Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10: 19-26.
    Pubmed CrossRef
  31. Zhang Q, Yu H, Tong T, Tong W, Dong L, Xu M, Wang Z. 2014. Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish Shellfish Immun. 38: 7-14.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(7): 1084-1092

Published online July 28, 2015 https://doi.org/10.4014/jmb.1501.01022

Copyright © The Korean Society for Microbiology and Biotechnology.

Prebiotic Potential of Xylooligosaccharides Derived from Corn Cobs and Their In Vitro Antioxidant Activity When Combined with Lactobacillus

Xiuhua Yu 1, 2, Jianyuan Yin 1, Lin Li 2, Chang Luan 3, Jian Zhang 3, Chunfang Zhao 1 and Shengyu Li 3*

1School of Pharmaceutical Sciences, Jilin University, Changchun 130021, P.R. China, 2The Affiliated Hospital to Changchun University of Chinese Medicine, Changchun 130021, P.R. China, 3Institute of Agro-food Technology, Jilin Academy of Agricultural Sciences, Changchun 130033, P.R. China

Received: January 12, 2015; Accepted: March 3, 2015

Abstract

In the present work, the in vitro prebiotic activity of xylooligosaccharides (XOS) derived from
corn cobs combined with Lactobacillus plantarum, a probiotic microorganism, was determined.
These probiotics exhibited different growth characteristics depending on strain specificity.
L. plantarum S2 cells were denser and their growth rates were higher when cultured on XOS.
Acetate was found to be the major short-chain fatty acid produced as the end-product of
fermentation, and its amount varied from 1.50 to 1.78 mg/ml. The antimicrobial activity of
XOS combined with L. plantarum S2 was determined against gastrointestinal pathogens. The
results showed that XOS proved to be an effective substrate, enhancing antimicrobial activity
for L. plantarum S2. In vivo evaluation of the influence of XOS and L. plantarum S2, used both
alone and together, on the intestinal microbiota in a mouse model showed that XOS combined
with L. plantarum S2 could increase the viable lactobacilli and bifidobacteria in mice feces and
decrease the viable Enterococcus, Enterobacter, and Clostridia spp. Furthermore, in the in vitro
antioxidant assay, XOS combined with L. plantarum S2 possessed significant 2,2-diphenyl-1-
picrylhydrazyl, 2,2’-azino-bis, and superoxide anion radical-scavenging activities, and the
combinations showed better antioxidant activity than either XOS or L. plantarum S2 alone.

Keywords: xylooligosaccharide, Lactobacillus plantarum, prebiotic, probiotic, antioxidant activity

References

  1. Connolly ML, Lovegrove JA, Tuohy KM. 2010. Konjac glucomannan hydrolysate beneficially modulates bacterial composition and activity within the faecal microbiota. J. Funct. Foods 2: 219-224.
    CrossRef
  2. Duangkaewmanee S, Petsom A. 2011. Synergistic and antagonistic effects on oxidation stability of antioxidants in a synthetic ester based oil. Tribol. Int. 44: 266-271.
    CrossRef
  3. Ferrario C, Taverniti V , Milani C, Fiore W, Laureati M, De Noni I, et al. 2014. Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillus paracasei DG varies among healthy adults. J. Nutr. 144: 17871796.
    Pubmed CrossRef
  4. Kao TH, Chen BH. 2006. Functional components in soybean cake and their effects on antioxidant activity. J. Agric. Food Chem. 54: 7544-7555.
    Pubmed CrossRef
  5. Kimmel SA, Roberts RF. 1998. Development of a growth medium suitable for exopolysaccharide production by Lactobacillus delbrueckii ssp. bulgaricus RR. Int. J. Food Microbiol. 40: 87-92.
    CrossRef
  6. Li M, Xu Y, Yang W, Li J, Xu X, Zhang X , et al. 2011. In vitro synergistic antioxidant activities of solvent-extracted fractions from Astragalus membranaceus and Glycyrrhiza uralensis. LWT Food Sci. Technol. 44: 1745-1751.
    CrossRef
  7. Likotrafiti E, Tuohy KM, Gibson GR, Rastall RA. 2014. An in vitro study of the effect of probiotics, prebiotics and synbiotics on the elderly faecal microbiota. Anaerobe 27: 50-55.
    Pubmed CrossRef
  8. Ma C, Feng M, Zhai X, Hu M, You L, Luo W, Zhao M. 2013. Optimization for the extraction of polysaccharides from Ganoderma lucidum and their antioxidant and antiproliferative activities. J. Taiwan Inst. Chem. E 44: 886-894.
    CrossRef
  9. Madhukumar MS, Muralikrishna G. 2010. Structural characterisation and determination of prebiotic activity of purified xylo-oligosaccharides obtained from Bengal gram husk (Cicer arietinum L.) and wheat bran (Triticum aestivum). Food Chem. 118: 215-223.
    CrossRef
  10. Makras L, Triantafyllou V , Messaoudi D F, Adriany T , Zoumpopoulou G, Tsakalidou E, et al. 2006. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res. Microbiol. 157: 241-247.
    Pubmed CrossRef
  11. Manisseri C, Gudipati M. 2010. Bioactive xylo-oligosaccharides from wheat bran soluble polysaccharides. LWT Food Sci. Technol. 43: 421-430.
    CrossRef
  12. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, et al. 2010. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302: 1-18.
    CrossRef
  13. Moura P, Cabanas S, Lourenco P, Girio F, Dias MCL, Esteves MP. 2008. In vitro fermentation of selected xylooligosaccharides by piglet intestinal microbiota. LWT Food Sci. Technol. 41: 1952-1961.
    CrossRef
  14. Moura P, Marques S, Alves J, Freire JPB, Cunha LF, Esteves MP. 2007. Effect of xylo-oligosaccharides from corn cobs autohydrolysis on the intestinal microbiota of piglets after weaning. Lives Sci. 108: 244-248.
    CrossRef
  15. Moure A, Gullón P, Domínguez H, Parajó JC. 2006. Advances in the manufacture, purification and applications of xylo-oligosaccharides as food additives and nutraceuticals. Process Biochem. 41: 1913-1923.
    CrossRef
  16. Muthu R, Thangavel P, Selvaraj N, Ramalingam R, Vaiyapuri M. 2013. Synergistic and individual effects of umbelliferone with 5-flurouracil on the status of lipid peroxidation and antioxidant defense against 1,2-dimethylhydrazine induced rat colon carcinogenesis. Biomed. Prev. Nutr. 3: 74-82.
    CrossRef
  17. Niki E. 2010. Assessment of antioxidant capacity in vitro and in vivo. Free Radical Biol. Med. 49: 503-515.
    Pubmed CrossRef
  18. Pan X , Wu T, Zhang L , Cai L , Song Z. 2 009. I nfluence o f oligosaccharides on the growth and tolerance capacity of lactobacilli to simulated stress environment. Lett. Appl. Microbiol. 48: 362-367.
    Pubmed CrossRef
  19. Ren T, Lu F, Zhang Y , Cheng Z , Xu M. 2010. I ntake of a high fat diet alters intestinal flora in rats. World J. Digest. 8: 2694-2697.
  20. 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.
    CrossRef
  21. Samanta K , Senani S, Kolte AP, Sridhar M, Sampath KT, Jayapal N, Devi A. 2009. Production and in vitro evaluationof xylooligosaccharides generated from corn cobs. Food Bioprod. Process. 90: 466-474.
    CrossRef
  22. Scheppach W, Luehrs H, Menzel T. 2001. Beneficial health effects of low-digestible carbohydrate consumption. Br. J. Nutr. 85: 23-30.
    CrossRef
  23. Schneider SM, Pipau FG, Anty R, Linde EGM, Geerling BJP, Knol J, et al. 2006. Effects of total enteral nutrition supplemented with a multi-fibre mix on faecal short-chain fatty acids and microbiota. Clin. Nutr. 25: 82-90.
    Pubmed CrossRef
  24. Shanks D, Maharik NA, Malmström J, Engman L, Eriksson P, Stenberg B, Reitberger T. 2003. Improved antioxidant formulations for polymeric materials – synergistic protective effects in combinations of organotellurium compounds with conventional phenolic antioxidants or thiols. Polym. Degrad. Stab. 81: 261-271.
    CrossRef
  25. Vrese M, Schrezenmeir JS. 2008. Probiotics, prebiotics, and synbiotics. Adv. Biochem. Eng. Biotechnol. 111: 1-66.
    Pubmed CrossRef
  26. Vulevic J, Rastall RA, Gibson GR. 2004. Developing a quantitative approach for determining the in vitro prebiotic potential of dietary oligosaccharides. FEMS Microbiol. Lett. 236: 153-159.
    Pubmed CrossRef
  27. Wang S, Meckling KA, Marcone MF, Kakuda Y, Proulx A, Tsao R. 2012. In vitro antioxidant synergism and antagonism between food extracts can lead to similar activities in H2O2induced cell death, caspase-3 and MMP-2 activities in H9c2 cells. J. Sci. Food Agric. 92: 2983-2993.
    Pubmed CrossRef
  28. Ye C, Hu W, Dai D. 2011. Extraction of polysaccharides and the antioxidant activity from the seeds of Plantago asiatica L. Int. J. Biol. Macromol. 49: 466-470.
    Pubmed CrossRef
  29. Yuan X, Wang J, Yao H. 2004. Antioxidant activity of feruloylated oligosaccharides from wheat bran. Food Chem. 90: 759-764.
    CrossRef
  30. Zampa A, Silvi S, Fabiani R, Morozzi G, Orpianesi C, Cresci A. 2004. Effects of different digestible carbohydrates on bile acid metabolism and SCFA production by human gut micro-flora grown in an in vitro semi-continuous culture. Anaerobe 10: 19-26.
    Pubmed CrossRef
  31. Zhang Q, Yu H, Tong T, Tong W, Dong L, Xu M, Wang Z. 2014. Dietary supplementation of Bacillus subtilis and fructooligosaccharide enhance the growth, non-specific immunity of juvenile ovate pompano, Trachinotus ovatus and its disease resistance against Vibrio vulnificus. Fish Shellfish Immun. 38: 7-14.
    Pubmed CrossRef