Yacon (Smallanthus sonchifolius) and Lactobacillus acidophilus CRL 1014 reduce the early phases of colon carcinogenesis in male Wistar rats

Food Research International

Volumn 74, Issue , 2015, Pages 48-54

  da Silva Almeida, Ana Paula ^a   Avi, Camilla Martins ^a   Barbisan, Luís Fernando ^a   de Moura, Nelci Antunes ^a   Caetano, Brunno Felipe Ramos ^a   Romualdo, Guilherme Ribeiro ^a   Sivieri, Kátia ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Chemical carcinogenesis; Colon; Prebiotic; Probiotic; Synbiotic

Indexed keywords

BACILLI; CELL DEATH; CELL PROLIFERATION; RATS; TUMORS;

1 ,2-DIMETHYLHYDRAZINE; CHEMOPREVENTIVE AGENTS; COLON; COLON CARCINOGENESIS; LACTOBACILLUS ACIDOPHILUS; PREBIOTICS; PROBIOTICS; SYNBIOTIC;

PATHOLOGY;

ANIMALIA; LACTOBACILLUS ACIDOPHILUS; POLYMNIA SONCHIFOLIA; RATTUS NORVEGICUS; SMALLANTHUS SONCHIFOLIUS;

EID: 84928652041     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2015.04.034     Document Type: Article

References (65)

1. [WHO] World Health Organization Cancer Fact sheet N° 297. Feb 2014 Available from:, (Accessed 02 Jul 2014). http://www.who.int/mediacentre/factsheets/fs297/en/.
2. Aybar M.J., Riera A.N.S., Grau A., Sa'nchez S.S. Hypoglycemic effect of the water extract of Smallantus sonchifolius (yacon) leaves in normal and diabetic rats. Journal of Ethnopharmacology 2001, 74:125-132.
3. Baldwin C., Millette M., Oth D., Ruiz M.T., Luquet F.M., Lacroix M. Probiotic Lactobacillus acidophilus and Lactobacillus casei mix sensitive colorectal tumoral cells to 5-fluorouracil-induced apoptosis. Nutrition and Cancer 2010, 62:371-378.
4. Bird R.P. Role of aberrant crypt foci in understand the pathogenesis of colon cancer. Cancer Letters 1995, 93:55-71.
5. Bolognani F., Rumn C.J., Pool-Zobel B., Rowland I.R. Effect of lactobacilli, bifidobacteria and inulin on the formation of aberrant crypt foci in rats. European Journal of Nutrition 2001, 40:293-300.
6. Campos D., Betalleluz-Pallardel I., Chirinos R., Aguilar-Galvez A., Noratto G., Pedreschi R. Prebiotic effects of yacon (Smallanthus sonchifolius Poepp. & Endl), a source of fructooligosaccharides and phenolic compounds with antioxidant activity. Food Chemistry 2012, 135:1592-1599.
7. Capurso G., Marignani M., Fave C.D. Probiotics and the incidence of colorectal cancer: When evidence is not evident. Digestive and Liver Disease 2006, 38:S277-S282.
8. Cheng T.C., Lai C.S., Chung M.C., Kalyanam N., Majeed M., Ho C.T., et al. Potent anti-cancer effect of 39 hydroxypterostilbene in human colon xenograft tumors. PLoS One 2014, 9:e111814.
9. Costa H., Lima F.O., Barrezueta L.F.M., Oshima C.T.F., Silva J.A., Gomes T.S., et al. Correlation between immunoexpression of BCL-2 protein family with apoptosis index, cellular proliferation and survival in colorectal carcinomas. Applied Cancer Research 2011, 31:74-80.
10. Costabile A.F., Fava H., Röytiö S.D., Forssten K., Olli J.K. Impact of polydextrose on the faecal microbiota: A double-blind, crossover, placebo-controlled feeding study in healthy human subjects. British Journal of Nutrition 2011, 108:471-481.
11. de Moura N.A., Caetano B.F.R., Sivieri K., Urbano L.H., Cabello C., Rodrigues M.A.M., et al. Protective effects of yacon (Smallanthus sonchifolius) intake on experimental colon carcinogenesis. Food and Chemical Toxicology 2012, 50:2902-2910.
12. de Preter V., Hamer H.M., Windey K., Verbeke K. The impact of pre- and/or probiotics on human colonic metabolism: Does it affect human health?. Molecular Nutrition & Food Research 2011, 55:46-57.
13. Delgado G.T.C., Thomé R., Gabriel D.L., Tamashiro W.M.S.C., Pastore G.M. Yacon (Smallanthus sonchifolius)-derived fructooligosaccharides improves the immune parameters in the mouse. Nutrition Research 2012, 32:884-892.
14. Dias M.C., Vieiralves N.F., Gomes M.I., Salvadori D.M., Rodrigues M.A., Barbisan L.F. Effects of lycopene, synbiotic and their association on early biomarkers of rat colon carcinogenesis. Food and Chemical Toxicology 2010, 48:772-780.
15. Food and Agriculture Organization of the United Nations, World Health Organization Evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria 2001, (Córdoba 34p. Available from: ftp://ftp.fao.org/docrep/fao/009/a0512e/a0512e00.pdf. Accessed 15 Sep 2011 [Report of a Joint FAO/WHO Expert Consultation]).
16. Fotiadis C.I., Stoidis C.N., Spyropoulus B.G., Zografos E.D. Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectalcancer. World Journal of Gastroenterology 2008, 14:6453-6645.
17. Genta S., Cabrera W., Habib N., Pons J., Carillo I.M., Grau A., et al. Yacon syrup: Beneficial effects on obesity and insulin resistance in humans. Clinical Nutrition 2009, 28:182-187.
18. Geyer M., Manrique I., Degen L., Beglinger C. Effect of yacon (Smallanthus sonchifolius) on colonic transit time in healthy volunteers. Digestion 2008, 78:30-33.
19. Habib N., Honoré S.M., Genta S.B., Sánchez S.S. Hypolipidemic effect of Smallanthus sonchifolius (yacon) roots on diabetic rats: Biochemical approach. Chemico-Biological Interactions 2011, 194:31-39.
20. Hamilton S.R., Aaltonen L.A. World health organization classification of tumours. Pathology and Genetics of Tumours of the Digestive System 2000, International Agency for Research for Cancer (IARC), (www.iarc.fr/en/publications/pdfs-online/pat-gen/bb2/index.php.).
21. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011, 144:646-674.
22. Hou N., Huo D., Dignam J.J. Prevention of colorectal cancer and dietary management. Chinese Clinical Oncology 2013, 2:2-13.
23. Hu Y., Martin J., Leu R.Le., Young G.P. The colonic response to genotoxic carcinogens in the rat: Regulation by dietary fibre. Carcinogenesis 2002, 23:1131-1137.
24. Humphries A., Wright N.A. Colonic crypt organization and tumorigenesis. Nature Review Cancer 2008, 8:415-424.
25. International Agency for Research on Cancer Globocan 2012: Estimated cancer incidence, mortality and prevalence worldwide in 2012 Available from:, (Accessed 02 jul 2014). http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx.
26. Khare S., Chaudhary K., Bissonnette M., Carroll R. Aberrant crypt foci in colon cancer epidemiology. Methods in Molecular Biology 2009, 472:373-386.
27. Kim Y., Oh S., Yun H.S., Oh S., Kim S.H. Cell-bound exopolysaccharide from probiotic bacteria induces autophagic cell death of tumor cells. Letters in Applied Microbiology 2010, 51:123-130.
28. Klaude M., Eriksson S., Nygren J., Ahnstrijm G. The comet assay: Mechanisms and technical considerations. Mutation Research 1996, 363:89-96.
29. Korakli M., Hinrichs C., Ehrmann M.A., Vogel R.F. Enzymatic determination of inulin and fructooligosaccharides in food. European Food Research and Technology 2003, 217:530-534.
30. Lee S.M., Lee W.K. Inhibitory effects of Lactic Acid Bacteria (LAB) on the azoxymethane induced colonic pre neoplastic lesions. The Journal of Microbiology 2000, 169-175.
31. Leu R.K.L., Brown I.L., Hu Y., Bird A.R., Jackson M., Esterman A., et al. A synbiotic combination of resistant starch and Bifidobacterium lactis facilitates apoptotic deletion of carcinogen-damaged cells in rat colon. Journal of Nutrition 2005, 996-1001.
32. Linsalata M., Russo F., Berloco P., Valentini A.M., Caruso M.L., Simone C., et al. Effects of probiotic bacteria (vsl#3) on the polyamine biosynthesis and cell proliferation of normal colonic mucosa of rats. In Vivo 2005, 19:989-996.
33. Liong M.T. Roles of probiotics and prebiotics in colon cancer prevention: postulated mechanisms and in-vivo evidence. International Journal of Molecular Sciences 2008, 9:854-863.
34. Liu C. Gastro-intestinal Sistem 2006, 453-458. Elsevier, Rio de Janeiro, (Chapter 17). 7th ed. R.N. Mitchell, V. Kumar, A.K. Abbas, N.R. Fausto, Cotran: Pathology Fundamentals (Eds.).
35. Lobo A.R., Colli C., Alvares E.P., Filisetti T.M.C.C. Effects of fructans-containing yacon (Smallanthus sonchifolius Poepp & Endl.) flour on caecum mucosal morphometry, calcium and magnesium balance, and bone calcium retention in growing rats. British Journal of Nutrition 2007, 97:776-785.
36. Lukin D.J., Carvajal L.A., Liu W.J., Resnick-Silverman L., Manfredi J.J. p53 Promotes cell survival due to the reversibility of its cell-cycle checkpoints. Molecular Cancer Research 2015, 1:16-28.
37. Ohyama W., Okada E., Fujiishi Y., Narumi K., Yasutake N. In vivo rat glandular stomach and colon micronucleus tests: Kinetics of micronucleated cells, apoptosis, and cell proliferation in the target issues after a single oral administration of stomach- or colon-carcinogens. Mutation Research 2013, 755:141-147.
38. Olive P.L., Banáth J.P. The comet assay: A method to measure DNA damage in individual cells. Nature Protocols 2006, 1:23-29.
39. Park J.S., Yang J.S., Hwang B.Y., Yoo B.Y., Han K. Hypoglycemic effect of yacon tuber extract and its constituent, chlorogenic acid, in streptozotocin-induced diabetic rats. Biomolecules & Therapeutics 2009, 17:256-262.
40. Pauly-Silveira N.D., Bedani R., Cavallini D.C.U., Manzoni M.S.J., Miguel D.P., Borsato D., et al. Optimization of a synbiotic formulation of soy yoghurt containing yacon extract by response surface methodology. International Journal of Probiotics and Prebiotics 2010, 5:175-182.
41. Perse M., Cerar A. Morphological and molecular alterations in 1,2 dimethylhydrazine and azoxymethane induced colon carcinogenesis in rats. Journal of Biomedicine and Biotechnology 2010, 1-14.
42. Pool-Zobel B.L. Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. British Journal of Nutrition 2005, 93:S73-S90.
43. Pool-Zobel B.L., Neudecker C., Domizlaff I., Ji S., Schillinger U., Rumney C., et al. Lactobacillus and Bifidobacterium mediated antigenotoxicity in the colon of rats. Nutrition and Cancer 1996, 26.
44. Rafter F., Bennett M., Caderni G., Clune Y., Hughes R., Karlsson P.C. Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. American Journal of Clinical Nutrition 2008, 85:488-496.
45. Rao C.V., Sanders M.E., Indranie C., Simi B., Reddy B.S. Prevention of colonic preneoplasic lesions by the probiotic Lactobacillus acidophilus NCFMTM in F344 rats. International Journal of Oncology 1999, 14:939-944.
46. Ravnik-Glavac M., Cerar A., Glavac D. Animal model in the study of colorectal carcinogenesis. Pflügers Archiv/European Journal of Physiology 2000, 440:R55-R57.
47. Roberfroid M.B. Prebiotics. Encyclopedia of food sciences and nutrition 2003, 4719-4723. Elsevier. 2nd ed.
48. Roselino M.N., Pauly-Silveira N.D., Cavallini D.C.U., Celiberto L.S., Pinto R.A., Vendramini R.C., et al. A potential synbiotic product improves the lipid profile of diabetic rats. Lipids in Health and Disease 2012, 11:2-9.
49. Rowland I.R., Bearne C.A., Fischer R., Pool-Zobel B.L. The effect of lactulose on DNA damage induced by DMH in the colon of human flora-associated rats. Nutrition and Cancer 1996, 26:37-47.
50. Sakuma K., Fujimori T., Hirabayashi K., Terano A. Cyclooxygenase (COX-2) immunoreactivity and relationship to p53 and ki-67 expression in colorectal cancer. Journal of Gastroenterology 1999, 34:189-194.
51. Santana I., Cardoso M.H. Yacon tuberous root (Smallanthus sonchifolius): cultivation potentialities, technological and nutritional aspects. Ciência Rural 2008, 38:898-905.
52. Singh N.P., Mccoy M.T., Tice R.R., Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 1988, 175:184-191.
53. Sivieri K., Morales M.V., Saad S.M.I., Adorno M.A., Sakamoto I.K., Rossi E.A. Prebiotic effect of fructooligosaccharide in the simulator of the human intestinal microbial ecosystem (SHIME model). Journal of Medicinal Food 2014, 17:1-8.
54. Sivieri K., Rossi E.A., Cano V.S.P., Valentine R.S. Survival of Enterococcus faecium CRL 183 through gastrointestinal transit in rats. Le Lait 2007, 87:59-69.
55. Sivieri K., Spinardi-Barbisan A.L.T., Barbisan L.F., Bedani R., Pauly N.D., Carlos I.Z., et al. Probiotic Enterococcus faecium CRL 183 inhibit chemically induced colon cancer in male Wistar rats. European Food Research and Technology 2008, 228:231-237.
56. Sivieri K., Villarreal M.L., Adorno M.A., Sakamoto I.K., Saad S.M., Rossi E.A. Lactobacillus acidophilus CRL 1014 improved 'gut health' in the SHIME(R) reactor. (2012). BMC Gastroenterology 2013, 13:100.
57. Takayama T., Katsuri S., Takahashi Y., Ohi M., Nojiri S., Sakamaki S., et al. Aberrant crypt foci of the colon as precursors of adenoma and cancer. New England Journal of Medicine 1998, 339:1277-1284.
58. Terzic J., Grivennikov S., Karin E., Karin M. Inflammation and colon cancer. Gastroenterology 2010, 138:2101-2114.
59. Tsamandas A.C., Kardamakis D., Tsiamalos P., Liava A., Tzelepi V., Vassiliou V., et al. The potential role of Bcl-2 expression, apoptosis and cell proliferation (Ki-67 expression) in cases of gastric carcinoma and correlation with classic prognostic factors and patient outcome. Anticancer Research 2009, 29:703-709.
60. Turner J.R. Gastro-intestinal Sistem 2012, 392-398. Elsevier, Rio de Janeiro, (Chapter 17). 8th ed. R.N. Mitchell, V. Kumar, A.K. Abbas, N. Fausto, J.C.R. Aster, Cotran: Pathology Fundamentals (Eds.).
61. Urbanska A.M., Bhathena J., Martoni C., Prakash S. Estimation of the potential antitumor activity of microencapsulated Lactobacillus acidophilus yogurt formulation in the attenuation of tumorigenesis in Apc (Min/+) mice. Digestive Diseases and Sciences 2009, 54:264-273.
62. Valentová K., Moncion A., Waziers I., Ulrichová J. The effect of Samallanthus sonshifolius leaf extracts on rat hepatic metabolism. Cell Biology and Toxicology 2004, 20:109-120.
63. Weinberg R.A. The Biology of Cancer 2007, Garland Science, Taylor & Francis Group, Michigan, (796p.).
64. Wu W.T., Yang L.C., Chen H.L. Effects of konjac glucomannan, inulin and cellulose on acute colonic responses to genotoxic azoxymethane. Food Chemistry 2014, 155:304-310.
65. Yan X., Suzuki M., Ohnishi-Kameyama M., Sada Y., Nakanishi T., Nagata T. Extraction and identification of antioxidants in the roots of yacon (Smallanthus sonchifolius). Journal of Agricultural and Food Chemistry 1999, 47:4711-4713.