Abstract
Inulin-rich foods exert a prebiotic effect, as this polysaccharide is able to enhance beneficial colon microbiota populations, giving rise to the in situ production of short-chain fatty acids (SCFAs) such as propionic and butyric acids. These SCFAs are potent preventive agents against colorectal cancer due to their histone deacetylases inhibitory properties, which induce apoptosis in tumor colonocytes. As colorectal cancer is the fourth most common neoplasia in Europe with 28.2 new cases per 100,000 inhabitants, a cost-effective preventive strategy has been tested in this work by redesigning common porcine meat products (chorizo sausages and cooked ham) consumed by a substantial proportion of the population towards potential colorectal cancer preventive functional foods. In order to test the preventive effect of these inulin-rich meat products against colorectal cancer, an animal model (Rattus norvegicus F344) was used, involving two doses of azoxymethane (10 mg/kg) and two treatments with dextran sodium sulfate (DSS) during a 20-week assay period. Control feed, control sausages, functional sausages (15.7% inulin), control cooked ham and functional cooked ham (10% inulin) were used to feed the corresponding animal cohorts. Then, the animals were sacrificed and their digestive tract tissues were analyzed. The results showed a statistically significant 49% reduction in the number of colon polyps in the functional meat products cohorts with respect to the control meat products animals, as well as an increase in the cecum weight (an indicator of a diet rich in prebiotic fiber), a 51.8% increase in colon propionate production, a 39.1% increase in colon butyrate concentrations, and a reduction in the number of hyperplastic Peyer’s patches. Metagenomics studies also demonstrated colon microbiota differences, revealing a significant increase in Bacteroidetes populations in the functional meat products (mainly due to an increase in Bacteroidaceae and Prevotellaceae families, which include prominent propionate producers), together with a reduction in Firmicutes (especially due to lower Lachnospiraceae populations). However, functional meat products showed a remarkable increase in the anti-inflammatory and fiber-fermentative Blautia genus, which belongs to this Lachnospiraceae family. The functional meat products cohorts also presented a reduction in important pro-inflammatory bacterial populations, such as those of the genus Desulfovibrio and Bilophila. These results were corroborated in a genetic animal model of CRC (F344/NSlc-Apc1588/kyo) that produced similar results. Therefore, processed meat products can be redesigned towards functional prebiotic foods of interest as a cost-effective dietary strategy for preventing colorectal cancer in human populations.
Highlights
Colorectal cancer (CRC) is the most common cancer in Western countries (35 cases per 100,000 inhabitants) and represents one of the leading causes of death[1]
Numerous epidemiological studies found a lower incidence of CRC in human populations with a high consumption of fruits and vegetables and low consumption of red meat and saturated fat[8]
Fructans usually contain 2 to 60 fructoses, and are called fructooligosaccharides or inulin[13,14,15,16]. Fructans such as inulin are not altered in the digestive tract of humans until they reach the colon, where they are used as a source of energy and carbon by the probiotic bacteria of the intestinal microbiota
Summary
Colorectal cancer (CRC) is the most common cancer in Western countries (35 cases per 100,000 inhabitants) and represents one of the leading causes of death[1]. Numerous epidemiological studies found a lower incidence of CRC in human populations with a high consumption of fruits and vegetables (which provide prebiotic fibers that, once fermented in the colon, give rise to short-chain fatty acids, SCFAs) and low consumption of red meat and saturated fat[8] These CRC tumorigenic processes in the colon mucosa (from the initial ACF to metastatic adenocarcinoma) can be altered or even stopped by the presence of some nutraceutical compounds in the colon lumen, such as prebiotic fibers. Fructans such as inulin are not altered in the digestive tract of humans until they reach the colon, where they are used as a source of energy and carbon by the probiotic bacteria of the intestinal microbiota Among these bacteria are lactic acid bacteria of the genera Bifidobacterium and Lactobacillus and other SCFAs producing species as a result of the fermentation of these prebiotic polysaccharides[17,18]. Dietary intake of inulin or other prebiotic fibers has been associated with a prevention or a reduction in the incidence of colon polyps and tumors, in the presence of bacteria able to ferment these polysaccharides, due to the generation of antitumor SCFAs23–25
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