Cooking Has Variable Effects on the Fermentability in the Large Intestine of the Fraction of Meats, Grain Legumes, and Insects That Is Resistant to Digestion in the Small Intestine in an in Vitro Model of the Pig’s Gastrointestinal Tract
in vitro method; pig; protein fermentation; short-chain fatty acid; hydrogen sulfide
Abstract :
[en] This study aimed to evaluate the fermentation in the large intestine of indigestible dietary protein sources from animal, insect, and plant origin using an in vitro model of the pig’s gastrointestinal tract. Protein sources were used raw and after a cooking treatment. Results showed that the category of the ingredient (meats, insects, or grain legumes) exerts a stronger impact on enzymatic digestibility, fermentation patterns, and bacterial metabolites such as short-chain fatty acids (SCFA) and hydrogen sulfide (H2S) than the cooking treatment. The digestibility and the fermentation characteristics of insects were more affected by the cooking procedure than the other categories. Per gram of consumed food, ingredients from animal origin, namely, meats and insects, were associated with fewer fermentation end-products (gas, H2S, SCFA) than ingredients from plant origin, which is related to their higher small intestinal digestibility.
Disciplines :
Food science
Author, co-author :
POELAERT, Christine ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Zootechnie
Despret, Xavier
Sindic, Marianne ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Laboratoire Qualité et sécurité des produits agro-aliment.
Beckers, Yves ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Zootechnie
Francis, Frédéric ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Portetelle, Daniel ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Microbiologie et génomique
Soyeurt, Hélène ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Statistique, Inform. et Mathém. appliquée à la bioingénierie
Thewis, André ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Zootechnie
Bindelle, Jérôme ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Zootechnie
Language :
English
Title :
Cooking Has Variable Effects on the Fermentability in the Large Intestine of the Fraction of Meats, Grain Legumes, and Insects That Is Resistant to Digestion in the Small Intestine in an in Vitro Model of the Pig’s Gastrointestinal Tract
Publication date :
2017
Journal title :
Journal of Agricultural and Food Chemistry
ISSN :
0021-8561
eISSN :
1520-5118
Publisher :
American Chemical Society, Washington, United States - District of Columbia
Volume :
65
Pages :
435-444
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
This research was supported by the Fund for Scientific Research (FNRS, Brussels, Belgium − Research Credit 1.5180.12). The research was performed within the framework of the collaborative Food4Gut excellence research program of the Walloon Government.
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique DGTRE - Région wallonne. Direction générale des Technologies, de la Recherche et de l'Énergie
Klurfeld, D. M. Research gaps in evaluating the relationship of meat and health. Meat Sci. 2015, 109, 86-95.
Rebello, C. J.; Greenway, F. L.; Finley, J. W. Whole grains and pulses: A comparison of the nutritional and health benefits. J. Agric. Food Chem. 2014, 62, 7029-7049.
Gerber, P. J.; Steinfeld, H.; Henderson, B.; Mottet, A.; Opio, C.; Dijkman, J.; Falcucci, A.; Tempio, G. Tackling Climate Change through Livestock: A Global Assessment of Emissions and Mitigation Opportunities; Food and Agriculture Organization of the United Nations (FAO): Rome, Italy, 2013.
Sánchez-Muros, M.-J.; Barroso, F. G.; Manzano-Agugliaro, F. Insect meal as renewable source of food for animal feeding: A review. J. Cleaner Prod. 2014, 65, 16-27.
Rumpold, B. A.; Schlüter, O. K. Potential and challenges of insects as an innovative source for food and feed production. Innovative Food Sci. Emerging Technol. 2013, 17, 1-11.
Chacko, A.; Cummings, J. H. Nitrogen losses from the human small bowel: obligatory losses and the effect of physical form of food. Gut 1988, 29, 809-815.
Cummings, J. H.; Macfarlane, G. T. Role of intestinal bacteria in nutrient metabolism. Clin. Nutr. 1997, 16, 3-11.
Silvester, K. R.; Cummings, J. H. Does digestibility of meat protein help explain large bowel cancer risk? Nutr. Cancer 1995, 24, 279-288.
Gilbert, J.-A.; Bendsen, N. T.; Tremblay, A.; Astrup, A. Effect of proteins from different sources on body composition. Nutr., Metab. Cardiovasc. Dis. 2011, 21, B16-B31.
Carbonaro, M.; Grant, G.; Cappelloni, M.; Pusztai, A. Perspectives into factors limiting in vivo digestion of legume proteins: Antinutritional compounds or storage proteins? J. Agric. Food Chem. 2000, 48, 742-749.
Gilani, G. S.; Wu Xiao, C.; Cockell, K. A. Impact of antinutritional factors in food proteins on the digestibility of protein and the bioavailability of amino acids and on protein quality. Br. J. Nutr. 2012, 108 (Suppl. 2), S315-S332.
Sante-Lhoutellier, V.; Aubry, L.; Gatellier, P. Effect of oxidation on in vitro digestibility of skeletal muscle myofibrillar proteins. J. Agric. Food Chem. 2007, 55, 5343-5348.
Macfarlane, G. T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int. 2012, 95, 50-60.
Cone, J. W.; Jongbloed, A. W.; Van Gelder, A. H.; de Lange, L. Estimation of protein fermentation in the large intestine of pigs using a gas production technique. Anim. Feed Sci. Technol. 2005, 123, 463- 472.
Macfarlane, G. T.; Gibson, G. R.; Beatty, E.; Cummings, J. H. Estimation of short-chain fatty acid production from protein by human intestinal bacteria based on branched-chain fatty acid measurements. FEMS Microbiol. Lett. 1992, 101, 81-88.
Windey, K.; De Preter, V.; Verbeke, K. Relevance of protein fermentation to gut health. Mol. Nutr. Food Res. 2012, 56, 184-196.
Pieper, R.; Villodre Tudela, C.; Taciak, M.; Bindelle, J.; Pérez, J. F.; Zentek, J. Health relevance of intestinal protein fermentation in young pigs. Anim. Health Res. Rev. 2016, 1.
Chao, A.; Thun, M. J.; Connell, C. J.; McCullough, M. L.; Jacobs, E. J.; Flanders, W. D.; Rodriguez, C.; Sinha, R.; Calle, E. E. Meat consumption and risk of colorectal cancer. JAMA 2005, 293, 172-182.
Yao, C. K.; Muir, J. G.; Gibson, P. R. Review article: insights into colonic protein fermentation, its modulation and potential health implications. Aliment. Pharmacol. Ther. 2016, 43, 181-196.
Hughes, R.; Kurth, M. J.; McGilligan, V.; McGlynn, H.; Rowland, I. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutr. Cancer 2008, 60, 259-266.
Andriamihaja, M.; Davila, A.-M.; Eklou-Lawson, M.; Petit, N.; Delpal, S.; Allek, F.; Blais, A.; Delteil, C.; Tomé, D.; Blachier, F. Colon luminal content and epithelial cell morphology are markedly modified in rats fed with a high-protein diet. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1030-G1037.
Attene-Ramos, M. S.; Wagner, E. D.; Plewa, M. J.; Gaskins, H. R. Evidence that hydrogen sulfide is a genotoxic agent. Mol. Cancer Res. 2006, 4, 9-14.
Pedersen, G.; Brynskov, J.; Saermark, T. Phenol toxicity and conjugation in human colonic epithelial cells. Scand. J. Gastroenterol. 2002, 37, 74-79.
Holmes, A. J.; Chew, Y. V.; Colakoglu, F.; Cliff, J. B.; Klaassens, E.; Read, M. N.; Solon-Biet, S. M.; McMahon, A. C.; Cogger, V. C.; Ruohonen, K.; Raubenheimer, D.; Le Couteur, D. G.; Simpson, S. J. Diet-microbiome interactions in health are controlled by intestinal nitrogen source constraints. Cell Metab. 2016, DOI:10.1016/j.cmet.2016.10.021.
Heinritz, S. N.; Mosenthin, R.; Weiss, E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr. Res. Rev. 2013, 26, 191-209.
Boccard, R.; Buchter, L.; Casteels, E.; Cosentino, E.; Dransfield, E.; Hood, D. E.; Joseph, R. L.; MacDougall, D. B.; Rhodes, D. N.; Schön, I.; Tinbergen, B. J.; Touraille, C. Procedures for measuring meat quality characteristics in beef production experiments. Report of a working group in the commission of the European Communities'(CEC) beef production research programme. Livest. Prod. Sci. 1981, 8, 385-397.
Bindelle, J.; Buldgen, A.; Boudry, C.; Leterme, P. Effect of inoculum and pepsin-pancreatin hydrolysis on fibre fermentation measured by the gas production technique in pigs. Anim. Feed Sci. Technol. 2007, 132, 111-122.
Boisen, S.; Fernandez, J. A. Prediction of the total tract digestibility of energy in feedstuffs and pig diets by in vitro analyses. Anim. Feed Sci. Technol. 1997, 68, 277-286.
Menke, K. H.; Steingass, H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 1988, 28, 7-55.
Poelaert, C.; Boudry, C.; Portetelle, D.; Théwis, A.; Bindelle, J. Use of medium without reducing agent for in vitro fermentation studies by bacteria isolated from pig intestine. J. Anim. Sci. 2012, 90(Suppl. 4), 387-389.
Mauricio, R. M.; Mould, F. L.; Dhanoa, M. S.; Owen, E.; Channa, K. S.; Theodorou, M. K. A semi- Automated in vitro gas production technique for ruminant feedstuff evaluation. Anim. Feed Sci. Technol. 1999, 79, 321-330.
Groot, J. C. J.; Cone, J. W.; Williams, B. A.; Debersaques, F. M. A.; Lantinga, E. A. Multiphasic analysis of gas production kinetics for in vitro fermentation of ruminant feeds. Anim. Feed Sci. Technol. 1996, 64, 77-89.
Leibovich, J.; Vasconcelos, J. T.; Galyean, M. L. Effects of corn processing method in diets containing sorghum wet distillers grain plus solubles on performance and carcass characteristics of finishing beef cattle and on in vitro fermentation of diets. J. Anim. Sci. 2009, 87, 2124-2132.
AOAC. Official Methods of Analysis, 15th ed.; Association of Official Analytical Chemists: Washington, DC, USA, 1990.
Van Soest, P. J.; Robertson, J. B.; Lewis, B. A. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 1991, 74, 3583-3597.
Bindelle, J.; Buldgen, A.; Delacollette, M.; Wavreille, J.; Agneessens, R.; Destain, J. P.; Leterme, P. Influence of source and concentrations of dietary fiber on in vivo nitrogen excretion pathways in pigs as reflected by in vitro fermentation and nitrogen incorporation by fecal bacteria. J. Anim. Sci. 2008, 87, 583-593.
Minekus, M.; Alminger, M.; Alvito, P.; Ballance, S.; Bohn, T.; Bourlieu, C.; Carriere, F.; Boutrou, R.; Corredig, M.; Dupont, D.; Dufour, C.; Egger, L.; Golding, M.; Karakaya, S.; Kirkhus, B.; Le Feunteun, S.; Lesmes, U.; Macierzanka, A.; Mackie, A.; Marze, S.; McClements, D. J.; Menard, O.; Recio, I.; Santos, C. N.; Singh, R. P.; Vegarud, G. E.; Wickham, M. S. J.; Weitschies, W.; Brodkorb, A. A standardised static in vitro digestion method suitable for food - An international consensus. Food Funct. 2014, 5, 1113-1124.
Kaur, L.; Maudens, E.; Haisman, D. R.; Boland, M. J.; Singh, H. Microstructure and protein digestibility of beef: The effect of cooking conditions as used in stews and curries. LWT-Food Sci. Technol. 2014, 55, 612-620.
Gatellier, P.; Santé-Lhoutellier, V. Digestion study of proteins from cooked meat using an enzymatic microreactor. Meat Sci. 2009, 81, 405-409.
Rist, V. T. S.; Weiss, E.; Eklund, M.; Mosenthin, R. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: A review. Animal 2013, 7, 1067-1078.
Davila, A.-M.; Blachier, F.; Gotteland, M.; Andriamihaja, M.; Benetti, P.-H.; Sanz, Y.; Tomé, D. Intestinal luminal nitrogen metabolism: Role of the gut microbiota and consequences for the host. Pharmacol. Res. 2013, 68, 95-107.
Leschelle, X.; Robert, V.; Delpal, S.; Mouillé, B.; Mayeur, C.; Martel, P.; Blachier, F. Isolation of pig colonic crypts for cytotoxic assay of luminal compounds: Effects of hydrogen sulfide, ammonia, and deoxycholic acid. Cell Biol. Toxicol. 2002, 18, 193-203.
Lewis, S.; Cochrane, S. Alteration of sulfate and hydrogen metabolism in the human colon by changing intestinal transit rate. Am. J. Gastroenterol. 2007, 102, 624-633.
Moughan, P. J. Amino acid availability: Aspects of chemical analysis and bioassay methodology. Nutr. Res. Rev. 2003, 16, 127-141.
Bender, A. Meat and Meat Products in Human Nutrition in Developing Countries; FAO: Rome, Italy, 1992.
Bravo, L.; Siddhuraju, P.; Saura-Calixto, F. Effect of various processing methods on the in vitro starch digestibility and resistant starch content of Indian pulses. J. Agric. Food Chem. 1998, 46, 4667- 4674.
Altay, F.; Gunasekaran, S. Influence of drying temperature, water content, and heating rate on gelatinization of corn starches. J. Agric. Food Chem. 2006, 54, 4235-4245.
Dongowski, G.; Jacobasch, G.; Schmiedl, D. Structural stability and prebiotic properties of resistant starch type 3 increase bile acid turnover and lower secondary bile acid formation. J. Agric. Food Chem. 2005, 53, 9257-9267.
Andrade, J. C.; Mandarino, J. M. G.; Kurozawa, L. E.; Ida, E. I. The effect of thermal treatment of whole soybean flour on the conversion of isoflavones and inactivation of trypsin inhibitors. Food Chem. 2016, 194, 1095-1101.
Mariotti, F.; Tomé, D.; Mirand, P. P. Converting nitrogen into protein - beyond 6.25 and Jones' factors. Crit. Rev. Food Sci. Nutr. 2008, 48, 177-184.
