Traditional Processed Meat Products Re-designed Towards Inulin-rich Functional Foods Reduce Polyps in Two Colorectal Cancer Animal Models

Scientific Reports

Volumn 9, Issue 1, 2019, Pages

  Fernández, Javier ^a,b   Ledesma, Estefanía ^c   Monte, Joaquín ^c   Millán, Enric ^d   Costa, Pedro ^d   de la Fuente, Vanessa García ^a   García, María Teresa Fernández ^a   Martínez Camblor, Pablo ^e   Villar, Claudio J ^a,b   Lombó, Felipe ^a,b  

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^b INSTITUTO DE INVESTIGACIÓN SANITARIA DEL PRINCIPADO DE ASTURIAS ISPA   (Spain)

^c El Hórreo Healthy Foods SL   (Spain)

^d El Hórreo Healthy Foods ^*  (Spain)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; DEXTRAN SULFATE; INULIN; PREBIOTIC AGENT; VOLATILE FATTY ACID;

ADMINISTRATION AND DOSAGE; ANIMAL; BIOSYNTHESIS; COLON; COLORECTAL TUMOR; DIETARY FIBER; EXPERIMENTAL NEOPLASM; FUNCTIONAL FOOD; GENETICS; HUMAN; INTESTINE FLORA; INTESTINE MUCOSA; INTESTINE POLYP; MALE; MEAT; METABOLISM; METAGENOMICS; MICROBIOLOGY; PATHOLOGY; PIG; RAT;

ANIMALS; AZOXYMETHANE; COLON; COLORECTAL NEOPLASMS; DEXTRAN SULFATE; DIETARY FIBER; FATTY ACIDS, VOLATILE; FUNCTIONAL FOOD; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINAL MUCOSA; INTESTINAL POLYPS; INULIN; MALE; MEAT PRODUCTS; METAGENOMICS; NEOPLASMS, EXPERIMENTAL; PREBIOTICS; RATS; SWINE;

EID: 85073468410     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-019-51437-w     Document Type: Article

References (90)

1. Jemal, A. et al. Global cancer statistics. CA. Cancer J. Clin. 61, 69–90 (2011).
2. Humphries, A. & Wright, N. A. Colonic crypt organization and tumorigenesis. Nat. Rev. Cancer 8, 415–24 (2008).
3. Bruce, W. R. & Corpet, D. E. The colonic protein fermentation and insulin resistance hypotheses for colon cancer etiology: experimental tests using precursor lesions. Eur. J. Cancer Prev. 5(Suppl 2), 41–7 (1996).
4. Kinzler, K. W. & Vogelstein, B. Lessons from hereditary colorectal cancer. Cell 87, 159–70 (1996).
5. Bouvard, V. et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 16, 1599–1600 (2015).
6. Sanchez-Diez, A., Hernandez-Mejia, R. & Cueto-Espinar, A. Study of the relation between diet and gastric cancer in a rural area of the Province of Leon, Spain. Eur. J. Epidemiol. 8, 233–7 (1992).
7. Serra Majem, L., Ribas Barba, L., Pérez Rodrigo, C., Roman Viñas, B. & Aranceta Bartrina, J. Dietary habits and food consumption in Spanish children and adolescents (1998–2000): socioeconomic and demographic factors. Med. Clin. (Barc). 121, 126–31 (2003).
8. Kim, Y. S. & Milner, J. A. Dietary modulation of colon cancer risk. J. Nutr. 137, 2576S–2579S (2007).
9. Gibson, G. R. et al. Dietary prebiotics: current status and new definition. Food Sci. Technol. Bull. Funct. Foods 7, 1–19 (2010).
10. Fernández, J. et al. Colon microbiota fermentation of dietary prebiotics towards short-chain fatty acids and their roles as anti-inflammatory and antitumour agents: A review. J. Funct. Foods 25, 511–522 (2016).
11. Comparot-Moss, S. & Denyer, K. The evolution of the starch biosynthetic pathway in cereals and other grasses. J. Exp. Bot. 60, 2481–92 (2009).
12. Ao, Z. et al. Evidence of native starch degradation with human small intestinal maltase-glucoamylase (recombinant). FEBS Lett. 581, 2381–8 (2007).
13. Cairns, A. J. Fructan biosynthesis in transgenic plants. J. Exp. Bot. 54, 549–67 (2003).
14. Vijn, I. & Smeekens, S. Fructan: more than a reserve carbohydrate? Plant Physiol. 120, 351–60 (1999).
15. Chi, Z.-M. et al. Biotechnological potential of inulin for bioprocesses. Bioresour. Technol. 102, 4295–303 (2011).
16. Fernández, J. et al. Healthy effects of prebiotics and their metabolites against intestinal diseases and colorectal cancer. AIMS Microbiol. 1, 48–71 (2015).
17. Roberfroid, M. B. Inulin-type fructans: functional food ingredients. J. Nutr. 137, 2493S–2502S (2007).
18. Bosscher, D., Breynaert, A., Pieters, L. & Hermans, N. Food-based strategies to modulate the composition of the intestinal microbiota and their associated health effects. J. Physiol. Pharmacol. 60(Suppl 6), 5–11 (2009).
19. Rumessen, J. J., Bodé, S., Hamberg, O. & Gudmand-Høyer, E. Fructans of Jerusalem artichokes: intestinal transport, absorption, fermentation, and influence on blood glucose, insulin, and C-peptide responses in healthy subjects. Am. J. Clin. Nutr. 52, 675–81 (1990).
20. Redondo-Blanco, S., Fernández, J., Gutiérrez-del-Río, I., Villar, C. J. & Lombó, F. New insights toward colorectal cancer chemotherapy using natural bioactive compounds. Front. Pharmacol. 8 (2017).
21. Hamer, H. M. et al. Review article: the role of butyrate on colonic function. Aliment. Pharmacol. Ther. 27, 104–19 (2008).
22. Zhang, J., Wu, G., Chapkin, R. S. & Lupton, J. R. Energy metabolism of rat colonocytes changes during the tumorigenic process and is dependent on diet and carcinogen. J. Nutr. 128, 1262–9 (1998).
23. Roller, M., Pietro Femia, A., Caderni, G., Rechkemmer, G. & Watzl, B. Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis. Br. J. Nutr. 92, 931–8 (2004).
24. Verghese, M., Walker, L. T., Shackelford, L. & Chawan, C. B. Inhibitory effects of nondigestible carbohydrates of different chain lengths on azoxymethane-induced aberrant crypt foci in Fisher 344 rats. Nutr. Res. 25, 859–868 (2005).
25. Donohoe, D. R. et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota- and butyrate-dependent manner. Cancer Discov. 4, 1387–97 (2014).
26. Amos-Landgraf, J. M. et al. A target-selected Apc-mutant rat kindred enhances the modeling of familial human colon cancer. Proc. Natl. Acad. Sci. 104, 4036–4041 (2007).
27. Irving, A. A. et al. The utility of Apc-mutant rats in modeling human colon cancer. Dis. Model. Mech. 7, 1215–25 (2014).
28. Mashimo, T. et al. An ENU-induced mutant archive for gene targeting in rats. Nat. Genet. 40, 514–5 (2008).
29. Yoshimi, K. et al. Enhanced colitis-associated colon carcinogenesis in a novel Apc mutant rat. Cancer Sci. 100, 2022–2027 (2009).
30. Fernández, J., García, L., Monte, J., Villar, C. J. & Lombó, F. Functional anthocyanin-rich sausages diminish colorectal cancer in an animal model and reduce pro-inflammatory bacteria in the intestinal microbiota. Genes (Basel). 9 (2018).
31. Heerdt, B. G., Houston, M. A. & Augenlicht, L. H. Short-chain fatty acid-initiated cell cycle arrest and apoptosis of colonic epithelial cells is linked to mitochondrial function. Cell Growth Differ. 8, 523–32 (1997).
32. Chen, J., Zhao, K.-N. & Vitetta, L. Effects of Intestinal Microbial–Elaborated Butyrate on Oncogenic Signaling Pathways. Nutrients 11, 1–26 (2019).
33. Archer, S. Y. & Hodint, R. A. Histone acetylation and cancer. Curr. Opin. Genet. Dev. 9, 171–174 (1999).
34. Struhl, K. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 12, 599–606 (1998).
35. Wilson, A. J. et al. Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Res. 70, 609–20 (2010).
36. Fernández, J. Healthy effects of prebiotics and their metabolites against intestinal diseases and colorectal cancer. AIMS Microbiol. 1, 48–71 (2015).
37. Roberfroid, M. et al. Prebiotic effects: metabolic and health benefits. Br. J. Nutr. 104(Suppl), S1–63 (2010).
38. Ledesma, E., Rendueles, M. & Díaz, M. Benzo(a)pyrene penetration on a smoked meat product during smoking time. Food Addit. Contam. Part A. Chem. Anal. Control. Expo. Risk Assess. 31, 1688–98 (2014).
39. Goldberg, I. J. Fat in the Blood, Fat in the Artery, Fat in the Heart: Triglyceride in Physiology and Disease. Arterioscler. Thromb. Vasc. Biol. 38, 700–706 (2018).
40. Scordo, K. & Pickett, K. A. CE: Triglycerides: Do They Matter? AJN, Am. J. Nurs. 117, 24–31 (2017).
41. Pereira, D. I. A. & Gibson, G. R. Effects of Consumption of Probiotics and Prebiotics on Serum Lipid Levels in Humans. Crit. Rev. Biochem. Mol. Biol. 37, 259–281 (2002).
42. Mishra, S. et al. Deoxynivalenol induced mouse skin cell proliferation and inflammation via MAPK pathway. Toxicol. Appl. Pharmacol. 279, 186–97 (2014).
43. Bailey, M. et al. Regulation of mucosal immune responses in effector sites. Proc. Nutr. Soc. 60, 427–435 (2001).
44. Jung, C., Hugot, J.-P. & Barreau, F. Peyer’s Patches: The Immune Sensors of the Intestine. Int. J. Inflam. 2010, 1–12 (2010).
45. Schulz, O. et al. Hypertrophy of infected Peyer’s patches arises from global, interferon-receptor, and CD69-independent shutdown of lymphocyte egress. Mucosal Immunol. 7, 892–904 (2014).
46. Xiao, J., Metzler-Zebeli, B. & Zebeli, Q. Gut Function-Enhancing Properties and Metabolic Effects of Dietary Indigestible Sugars in Rodents and Rabbits. Nutrients 7, 8348–8365 (2015).
47. Cummings, J. H., Macfarlane, G. T. & Englyst, H. N. Prebiotic digestion and fermentation. Am. J. Clin. Nutr. 73, 415s–420s (2001).
48. Qamar, T. et al. Novel Combination of Prebiotics Galacto-Oligosaccharides and Inulin-Inhibited Aberrant Crypt Foci Formation and Biomarkers of Colon Cancer in Wistar Rats. Nutrients 8, 465 (2016).
49. Moen, B. et al. Effect of Dietary Fibers on Cecal Microbiota and Intestinal Tumorigenesis in Azoxymethane Treated A/J Min/+ Mice. PLoS One 11, e0155402 (2016).
50. Yang, J. & Yu, J. The association of diet, gut microbiota and colorectal cancer: what we eat may imply what we get. Protein Cell 9, 474–487 (2018).
51. Ley, R. E. et al. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. 102, 11070–11075 (2005).
52. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–3 (2006).
53. Reygner, J. et al. Inulin Supplementation Lowered the Metabolic Defects of Prolonged Exposure to Chlorpyrifos from Gestation to Young Adult Stage in Offspring Rats. PLoS One 11, e0164614 (2016).
54. Van den Abbeele, P., Venema, K., Van de Wiele, T., Verstraete, W. & Possemiers, S. Different Human Gut Models Reveal the Distinct Fermentation Patterns of Arabinoxylan versus Inulin. J. Agric. Food Chem. 61, 9819–9827 (2013).
55. Ferrario, C. et al. How to Feed the Mammalian Gut Microbiota: Bacterial and Metabolic Modulation by Dietary Fibers. Front. Microbiol. 8 (2017).
56. Polansky, O. et al. Important Metabolic Pathways and Biological Processes Expressed by Chicken Cecal Microbiota. Appl. Environ. Microbiol. 82, 1569–1576 (2016).
57. Flemer, B., Herlihy, M., O’Riordain, M., Shanahan, F. & O’Toole, P. W. Tumour-associated and non-tumour-associated microbiota: Addendum. Gut Microbes 1–5, https://doi.org/10.1080/19490976.2018.1435246 (2018).
58. Weir, T. L. et al. Stool Microbiome and Metabolome Differences between Colorectal Cancer Patients and Healthy Adults. PLoS One 8, e70803 (2013).
59. Zackular, J. P. et al. The Gut Microbiome Modulates Colon Tumorigenesis. MBio 4 (2013).
60. Zhu, Q. et al. Analysis of the Intestinal Lumen Microbiota in an Animal Model of Colorectal Cancer. PLoS One 9, e90849 (2014).
61. Voreades, N., Kozil, A. & Weir, T. L. Diet and the development of the human intestinal microbiome. Front. Microbiol. 5 (2014).
62. Sun, J. & Kato, I. Gut microbiota, inflammation and colorectal cancer. Genes Dis. 3, 130–143 (2016).
63. Dai, Z. et al. Multi-cohort analysis of colorectal cancer metagenome identified altered bacteria across populations and universal bacterial markers. Microbiome 6, 70 (2018).
64. Catry, E. et al. Targeting the gut microbiota with inulin-type fructans: preclinical demonstration of a novel approach in the management of endothelial dysfunction. Gut 67, 271–283 (2018).
65. Sanchez, M., Panahi, S. & Tremblay, A. Childhood Obesity: A Role for Gut Microbiota? Int. J. Environ. Res. Public Health 12, 162–175 (2014).
66. Jenq, R. R. et al. Intestinal Blautia Is Associated with Reduced Death from Graft-versus-Host Disease. Biol. Blood Marrow Transplant. 21, 1373–1383 (2015).
67. Neyrinck, A. M. et al. Intestinal Sucrase as a Novel Target Contributing to the Regulation of Glycemia by Prebiotics. PLoS One 11, e0160488 (2016).
68. Tannock, G. W. et al. RNA–Stable-Isotope Probing Shows Utilization of Carbon from Inulin by Specific Bacterial Populations in the Rat Large Bowel. Appl. Environ. Microbiol. 80, 2240–2247 (2014).
69. Chen, W., Liu, F., Ling, Z., Tong, X. & Xiang, C. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 7 (2012).
70. Bhattacharyya, A. et al. Graft-Derived Reconstitution of Mucosal-Associated Invariant T Cells after Allogeneic Hematopoietic Cell Transplantation. Biol. Blood Marrow Transplant. 24, 242–251 (2018).
71. Toscano, M., De Grandi, R., Stronati, L., De Vecchi, E. & Drago, L. Effect of Lactobacillus rhamnosus HN001 and Bifidobacterium longum BB536 on the healthy gut microbiota composition at phyla and species level: A preliminary study. World J. Gastroenterol. 23, 2696 (2017).
72. Chua, H.-H. et al. Intestinal Dysbiosis Featuring Abundance of Ruminococcus gnavus Associates With Allergic Diseases in Infants. Gastroenterology 154, 154–167 (2018).
73. Hall, A. B. et al. A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients. Genome Med. 9, 1–12 (2017).
74. Haenen, D. et al. A Diet High in Resistant Starch Modulates Microbiota Composition, SCFA Concentrations, and Gene Expression in Pig Intestine. J. Nutr. 143, 274–283 (2013).
75. Sokol, H. et al. Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm. Bowel Dis. 12, 106–111 (2006).
76. Palaria, A., Johnson-Kanda, I. & O’Sullivan, D. J. Effect of a Synbiotic Yogurt on Levels of Fecal Bifidobacteria, Clostridia, and Enterobacteria. Appl. Environ. Microbiol. 78, 933–940 (2012).
77. Zhang, S. et al. Dietary pomegranate extract and inulin affect gut microbiome differentially in mice fed an obesogenic diet. Anaerobe 48, 184–193 (2017).
78. Zhang, W. et al. Oral Administration of a Select Mixture of Bacillus Probiotics Affects the Gut Microbiota and Goblet Cell Function following Escherichia coli Challenge in Newly Weaned Pigs of Genotype MUC4 That Are Supposed To Be Enterotoxigenic E. coli F4ab/ac Receptor. Appl. Environ. Microbiol. 83 (2017).
79. Yang, J., Martínez, I., Walter, J., Keshavarzian, A. & Rose, D. J. In vitro characterization of the impact of selected dietary fibers on fecal microbiota composition and short chain fatty acid production. Anaerobe 23, 74–81 (2013).
80. Zhang, Q. et al. Inulin-type fructan improves diabetic phenotype and gut microbiota profiles in rats. PeerJ 6, e4446 (2018).
81. Citronberg, J. S. et al. Association of gut microbial communities with plasma lipopolysaccharide-binding protein (LBP) in premenopausal women. ISME J. 12, 1631–1641 (2018).
82. Chen, Y. et al. Wuji Wan Formula Ameliorates Diarrhea and Disordered Colonic Motility in Post-inflammation Irritable Bowel Syndrome Rats by Modulating the Gut Microbiota. Front. Microbiol. 8 (2017).
83. Kreutzer, C. et al. Hypothalamic Inflammation in Human Obesity Is Mediated by Environmental and Genetic Factors. Diabetes 66, 2407–2415 (2017).
84. Deng, Y.-F. et al. Efficacy and role of inulin in mitigation of enteric sulfur-containing odor in pigs. J. Sci. Food Agric. 97, 2382–2391 (2017).
85. Song, H. et al. Pretreatment with probiotic Bifico ameliorates colitis-associated cancer in mice: Transcriptome and gut flora profiling. Cancer Sci. 109, 666–677 (2018).
86. Thomas, A. M. et al. Tissue-Associated Bacterial Alterations in Rectal Carcinoma Patients Revealed by 16S rRNA Community Profiling. Front. Cell. Infect. Microbiol. 6 (2016).
87. Devkota, S. et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487, 104–8 (2012).
88. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–63 (2014).
89. Yazici, C. et al. Race-dependent association of sulfidogenic bacteria with colorectal cancer. Gut 66, 1983–1994 (2017).
90. Fernández, J. et al. A Galacto-Oligosaccharides Preparation Derived From Lactulose Protects Against Colorectal Cancer Development in an Animal Model. Front. Microbiol. 9, 2004 (2018).