The DOI matches its Crossref record; 106 of the 106 references it cites were found in a registry or an index.
Relevance of protein fermentation to gut health
Abstract
It is generally accepted that carbohydrate fermentation results in beneficial effects for the host because of the generation of short chain fatty acids, whereas protein fermentation is considered detrimental for the host's health. Protein fermentation mainly occurs in the distal colon, when carbohydrates get depleted and results in the production of potentially toxic metabolites such as ammonia, amines, phenols and sulfides. However, the effectivity of these metabolites has been established mainly in in vitro studies. In addition, some important bowel diseases such as colorectal cancer (CRC) and ulcerative colitis appear most often in the distal colon, which is the primary site of protein fermentation. Finally, epidemiological studies revealed that diets rich in meat are associated with the prevalence of CRC, as is the case in Western society. Importantly, meat intake not only increases fermentation of proteins but also induces increased intake of fat, heme and heterocyclic amines, which may also play a role in the development of CRC. Despite these indications, the relationship between gut health and protein fermentation has not been thoroughly investigated. In this review, the existing evidence about the potential toxicity of protein fermentation from in vitro animal and human studies will be summarized.
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In the citing paper
“Studies in animal models and in vitro show that compounds like ammonia, phenols, p-cresol, certain amines and hydrogen sulfide, play important roles in the initiation or progression of a leaky gut, inflammation, DNA damage and cancer progression.15”
From The gut microbiota and host health: a new clinical frontier (2016) · cites this paper as [15]
In the citing paper
“Regarding this, as protein consumption is increased, the amount of proteins reaching the colon is increasing correspondingly, leading to numerous and diverse bacterial metabolite production (e.g., hydrogen sulfide, branched-chain fatty acids (BCFAs), SCFAs, polyamines, ammonia, methane, aromatic compounds, nitric oxide, tyramine, tryptamine, phenethylamine, serotonin, histamine, and others) in the”
From Impact of Protein Intake in Older Adults with Sarcopenia and Obesity: A Gut Microbiota Perspective (2020) · cites this paper as [147]
In the citing paper
“BCAA deamination leading to BCFA production is a marker of colonic fermentation developed by protein consumption [147].”
From Impact of Protein Intake in Older Adults with Sarcopenia and Obesity: A Gut Microbiota Perspective (2020) · cites this paper as [147]
In the citing paper
“Fermented foods enriched with Lactobacillus sp. and Bifidobacteria sp [129] can result in specific changes in gut microbiota activity, improving stress-induced symptoms such as depression, mood disturbance as well as digestive issues [130].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [129]
In the citing paper
“While athletes may require a higher protein intake, high protein diets can affect the microbiota composition and function through amino acid fermentation in the colon that produces undesirable metabolites (e.g. phenol, hydrogen sulfide and amines) and urea and tend to lead to higher fecal pH (reviewed by Windey et al [129]).”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [129]
Citations
Cites
Food, nutrition, physical activity, and the prevention of cancer: a global perspective
Marmot, M. G., Atinmo, T., Byers, T., Chen, J., Hirohata, T., Jackson, A., James, W., Kolonel, L. N., Kumanyika, S., Leitzmann, C., et al. (2008) · Choice Reviews Online · doi:10.5860/choice.45-5024 · Cited by 5,368
Amino acids: Metabolism, functions, and nutrition
Wu, G. (2009) · Amino Acids · doi:10.1007/s00726-009-0269-0 · Cited by 3,004
Review article: the role of butyrate on colonic function
HAMER, H. M., JONKERS, D., VENEMA, K., VANHOUTVIN, S., TROOST, F. J., & BRUMMER, R. ‐. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2007.03562.x · Cited by 2,721
Willett, W. C., Stampfer, M. J., Colditz, G. A., ROSNER, B. A., & Speizer, F. E. (1990) · New England Journal of Medicine · doi:10.1056/nejm199012133232404 · Cited by 1,239
Hou, J. K., Abraham, B., & El-Serag, H. (2011) · American Journal of Gastroenterology · doi:10.1038/ajg.2011.44 · Cited by 1,009
Toxicology Of Hydrogen Sulfide
Reiffenstein, R. J., Hulbert, W. C., & Roth, S. (1992) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.32.040192.000545 · Cited by 971
Norat, T., Bingham, S. A., Ferrari, P., Slimani, N., Jenab, M., Mazuir, M., Overvad, K., Olsen, A., Tjønneland, A. M., Clavel‐Chapelon, F., et al. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji164 · Cited by 875
Primary Prevention of Colorectal Cancer
Chan, A. T., & Giovannucci, E. L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.01.057 · Cited by 758
Intake of fat, meat, and fiber in relation to risk of colon cancer in men.
Giovannucci, E. L., Rimm, E. B., Stampfer, M. J., Colditz, G. A., Ascherio, A., & Willett, W. C. (1994) · PubMed · Cited by 694
Comparison of fermentation reactions in different regions of the human colon
Macfarlane, G. T., Gibson, G. R., & Cummings, J. H. (1992) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1992.tb04882.x · Cited by 676
BACTERIA AND qTIOLOGY OF CANCER OF LARGE BOWEL
Hill, M. J. (1971) · The Lancet · doi:10.1016/s0140-6736(71)90837-3 · Cited by 631
Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients
Rafter, J. J., Bennett, M., Caderni, G., Clune, Y., Hughes, R., Karlsson, P. C., Klinder, A., O'Riordan, M., O’Sullivan, G. C., Pool-Zobel, B. L., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.2.488 · Cited by 601
Meat consumption and risk of colorectal cancer.
Chao, A., Thun, M., Connell, C., McCullough, M., Jacobs, E., Flanders, W., Rodríguez, C., Sinha, R., & Calle, E. (2005) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.293.2.172 · Cited by 569
Manning, T. S., & Gibson, G. R. (2004) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2003.10.008 · Cited by 480
Protein Degradation by Human Intestinal Bacteria
Macfarlane, G. T., Cummings, J. H., & Allison, C. (1986) · Microbiology · doi:10.1099/00221287-132-6-1647 · Cited by 455
Blachier, F., Mariotti, F., Huneau, J. F., & Tomé, D. (2007) · Amino Acids · doi:10.1007/s00726-006-0477-9 · Cited by 452
Shoda, R., Matsueda, K., Yamato, S., & Umeda, N. (1996) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.5.741 · Cited by 444
Animal Protein Intake and Risk of Inflammatory Bowel Disease: The E3N Prospective Study
Jantchou, P., Morois, S., Clavel‐Chapelon, F., Boutron‐Ruault, M., & Carbonnel, F. (2010) · The American Journal of Gastroenterology · doi:10.1038/ajg.2010.192 · Cited by 441
Dissimilatory Amino Acid Metabolism in Human Colonic Bacteria
Smith, E. A., & Macfarlane, G. T. (1997) · Anaerobe · doi:10.1006/anae.1997.0121 · Cited by 388
Evidence That Hydrogen Sulfide Is a Genotoxic Agent
Attene‐Ramos, M. S., Wagner, E. D., Plewa, M. J., & Gaskins, H. R. (2006) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-05-0126 · Cited by 367
Magee, E. A., Richardson, C. J., Hughes, R., & Cummings, J. H. (2000) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/72.6.1488 · Cited by 359
Microbial Degradation Products Influence Colon Cancer Risk: the Butyrate Controversy
Lupton, J. R. (2004) · Journal of Nutrition · doi:10.1093/jn/134.2.479 · Cited by 343
Gastrointestinal microflora, food components and colon cancer prevention
Davis, C. D., & Milner, J. A. (2009) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.06.001 · Cited by 340
Diet and risk of colorectal cancer in a cohort of Finnish men
Pietinen, P., Malila, N. K., Virtanen, M. J., Hartman, T. J., Tangrea, J. A., Albanes, D., & Virtamo, J. R. K. (1999) · Cancer Causes & Control · doi:10.1023/a:1008962219408 · Cited by 339
Pitcher, M. (2000) · Gut · doi:10.1136/gut.46.1.64 · Cited by 297
Changes in fecal composition and colonic function due to cereal fiber
Cummings, J., Hill, M. J., Jenkins, D. J. A., Pearson, J., & Hs, W. (1976) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/29.12.1468 · Cited by 287
Hydrogen Sulfide Induces Direct Radical-Associated DNA Damage
Attene‐Ramos, M. S., Wagner, E. D., Gaskins, H. R., & Plewa, M. J. (2007) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-06-0439 · Cited by 277
Protein degradation in the large intestine: relevance to colorectal cancer.
Hughes, R., Magee, E., & Bingham, S. A. (2000) · PubMed · Cited by 271
Colonic Sulfide in Pathogenesis and Treatment of Ulcerative Colitis
Roediger, W. E. W., Moore, J., & Babidge, W. (1997) · Digestive Diseases and Sciences · doi:10.1023/a:1018851723920 · Cited by 270
Tricker, A. R. (1997) · European Journal of Cancer Prevention · doi:10.1097/00008469-199706000-00003 · Cited by 268
The Western-style diet: a major risk factor for impaired kidney function and chronic kidney disease
Odermatt, A. (2011) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00068.2011 · Cited by 262
A prospective cohort study on the relation between meat consumption and the risk of colon cancer.
Goldbohm, R. A., van den Brandt, P. A., Veer, P. V. ’., Brants, H. A. M., Dorant, E., STURMANS, F., & Hermus, R. J. J. (1994) · PubMed · Cited by 261
Influence of dietary protein supplements on the formation of bacterial metabolites in the colon.
Geypens, B. J., Claus, D., Evenepoel, P., Hiele, M. I., Maes, B., Peeters, M., Rutgeerts, P., & Ghoos, Y. F. (1997) · Gut · doi:10.1136/gut.41.1.70 · Cited by 245
Attene‐Ramos, M. S., Nava, G. M., Muellner, M. G., Wagner, E. D., Plewa, M. J., & Gaskins, H. R. (2010) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20546 · Cited by 244
Resistant starch lowers fecal concentrations of ammonia and phenols in humans
Birkett, A., Muir, J. G., Phillips, J. R., Jones, G., & O’Dea, K. (1996) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/63.5.766 · Cited by 241
Diet and cell growth modulation by ammonia
Visek, W. J. (1978) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/31.10.s216 · Cited by 237
Case‐control study of proximal and distal colon cancer and diet in Wisconsin
Young, T. B., & Wolf, D. A. (1988) · International Journal of Cancer · doi:10.1002/ijc.2910420205 · Cited by 234
Effects of Lactulose and Lactitol on Colonic Microflora and Enzymatic Activity
Ballongue, J., Schumann, C., & Quignon, P. (1997) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.1997.11720716 · Cited by 233
Ling, W. H., Korpela, R., Mykkänen, H. M., Salminen, S., & Hänninen, O. (1994) · Journal of Nutrition · doi:10.1093/jn/124.1.18 · Cited by 212
Effect of proteins from different sources on body composition
Gilbert, J.-A., Bendsen, N. T., Tremblay, A., & Astrup, A. (2011) · Nutrition, Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2010.12.008 · Cited by 207
Younes, H., Garleb, K. A., Behr, S. R., Rémésy, C., & Demigné, C. (1995) · Journal of Nutrition · doi:10.1093/jn/125.4.1010 · Cited by 197
Deplancke, B., & Gaskins, H. R. (2003) · The FASEB Journal · doi:10.1096/fj.02-0883fje · Cited by 190
Leschelle, X., Goubern, M., Andriamihaja, M., Blottière, H. M., Couplan, E., González‐Barroso, M. M., Petit, C., Pagniez, A., Chaumontet, C., Mignotte, B., et al. (2005) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2005.06.002 · Cited by 187
Preter, V. D., Vanhoutte, T., Huys, G. R. B., Swings, J., Vuyst, L. D., Rutgeerts, P. J., & Verbeke, K. (2006) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00052.2006 · Cited by 178
Self-citationImpact of a synbiotic food on the gut microbial ecology and metabolic profiles
Vitali, B., Ndagijimana, M., Cruciani, F., Carnevali, P., Candela, M., Guerzoni, M. E., & Brigidi, P. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-4 · Cited by 172
Venturi, M. (1997) · Carcinogenesis · doi:10.1093/carcin/18.12.2353 · Cited by 162
Dietary fat, cholesterol and colorectal cancer in a prospective study
Järvinen, R., Knekt, P., Hakulinen, T. R., Rissanen, H. A., & Heliövaara, M. (2001) · British Journal of Cancer · doi:10.1054/bjoc.2001.1906 · Cited by 162
Cloetens, L., Broekaert, W. F., Delaedt, Y., Ollevier, F., Courtin, C. M., Delcour, J. A., Rutgeerts, P. J., & Verbeke, K. (2009) · British Journal Of Nutrition · doi:10.1017/s0007114509992248 · Cited by 151
Self-citationAmount and fate of egg protein escaping assimilation in the small intestine of humans
Evenepoel, P., Claus, D., Geypens, B. J., Hiele, M. I., Geboes, K., Rutgeerts, P. J., & Ghoos, Y. F. (1999) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1999.277.5.g935 · Cited by 151
Worthley, D. L., Leu, R. K. L., Whitehall, V., Conlon, M. A., Christophersen, C. T., Belobrajdic, D. P., Mallitt, K., Hu, Y. C., Irahara, N., Ogino, S., et al. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28106 · Cited by 149
Diet-induced endogenous formation of nitroso compounds in the GI tract
Kuhnle, G. G. C., Story, G. W., Reda, T., Mani, A. R., Moore, K. P., Lunn, J. C., & Bingham, S. A. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.03.011 · Cited by 146
Andriamihaja, M., Davila, A., Eklou-Lawson, M., Petit, N., Delpal, S., Allek, F., Blais, A., Delteil, C., Tomé, D., & Blachier, F. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00149.2010 · Cited by 145
Emerging role of hydrogen sulfide in colonic physiology and pathophysiology
Medani, M., Collins, D., Docherty, N. G., Baird, A. W., O’Connell, P. R., & Winter, D. C. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21528 · Cited by 142
Diet in the Aetiology of Ulcerative Colitis: A European Prospective Cohort Study
Hart, A. R., Luben, R., Olsen, A., Tjønneland, A. M., Linseisen, J., Nagel, G., Berglund, G., Lindgren, S. C., Grip, O., Key, T. J., et al. (2008) · Digestion · doi:10.1159/000121412 · Cited by 141
Effect of Colonic Bacterial Metabolites on Caco-2 Cell Paracellular Permeability In Vitro
Hughes, R., Kurth, M. J., McGilligan, V., McGlynn, H., & Rowland, I. R. (2008) · Nutrition and Cancer · doi:10.1080/01635580701649644 · Cited by 139
McCall, I. C., Betanzos, A., Weber, D. A., Nava, P., Miller, G. W., & Parkos, C. A. (2009) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2009.08.002 · Cited by 133
Roediger, W. E. W., Duncan, A. J., Kapaniris, O., & Millard, S. M. (1993) · Clinical Science · doi:10.1042/cs0850623 · Cited by 130
Colon Mucosal Cell Damage by Ammonia in Rats
Lin, H.-C., & Visek, W. J. (1991) · Journal of Nutrition · doi:10.1093/jn/121.6.887 · Cited by 123
Does digestibility of meat protein help explain large bowel cancer risk?
Silvester, K. R., & Cummings, J. H. (1995) · Nutrition and Cancer · doi:10.1080/01635589509514417 · Cited by 114
Toden, S., Bird, A. R., Topping, D. L., & Conlon, M. A. (2006) · Cancer Biology & Therapy · doi:10.4161/cbt.5.3.2382 · Cited by 113
Meta-analysis of animal fat or animal protein intake and colorectal cancer
Alexander, D. D., Cushing, C. A., Lowe, K. A., Sceurman, B. K., & Roberts, M. A. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26838 · Cited by 112
Bartram, H.-P., Scheppach, W. M., Schmid, H. A., Hofmann, A. F., Dusel, G., Richter, F., Richter, A., & Kasper, H. (1993) · PubMed · Cited by 109
Effect of isomalt consumption on faecal microflora and colonic metabolism in healthy volunteers
Gostner, A., Blaut, M., Schäffer, V., Kozianowski, G., Theis, S., Klingeberg, M., Dombrowski, Y., Martin, D., Ehrhardt, S., Taras, D., et al. (2006) · British Journal Of Nutrition · doi:10.1079/bjn20051589 · Cited by 108
Red meat and colorectal cancer: a critical summary of prospective epidemiologic studies
Alexander, D. D., & Cushing, C. A. (2010) · Obesity Reviews · doi:10.1111/j.1467-789x.2010.00785.x · Cited by 107
Diet, fecal water, and colon cancer - development of a biomarker
Pearson, J. R., Gill, C. I., & Rowland, I. R. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.2009.00224.x · Cited by 103
Resistant Starch Attenuates Colonic DNA Damage Induced by Higher Dietary Protein in Rats
Toden, S., Bird, A. R., Topping, D. L., & Conlon, M. A. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5101_7 · Cited by 102
P-cresol, a uremic retention solute, alters the endothelial barrier function in vitro
Dou, L., Anfosso, F. J., Sabatier, F., Moal, V., Glorieux, G., Smet, R. D., Vanholder, R., Dignat‐George, F., Sampol, J., Berland, Y., et al. (2004) · Thrombosis and Haemostasis · doi:10.1160/th03-07-0491 · Cited by 99
Clinton, S. K., Bostwick, D. G., OLSON, L. M., Mangian, H. J., & Visek, W. J. (1988) · PubMed · Cited by 97
Toden, S., Bird, A. R., Topping, D. L., & Conlon, M. A. (2007) · Carcinogenesis · doi:10.1093/carcin/bgm216 · Cited by 92
Oberreuther-Moschner, D. L., Jahreis, G., Rechkemmer, G., & Pool-Zobel, B. L. (2004) · British Journal Of Nutrition · doi:10.1079/bjn20041108 · Cited by 92
Glinghammar, B., Venturi, M., Rowland, I. R., & Jj, R. (1997) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/66.5.1277 · Cited by 91
Rieger, M. A., Parlesak, A., Pool-Zobel, B. L., Rechkemmer, G., & Bode, C. (1999) · Carcinogenesis · doi:10.1093/carcin/20.12.2311 · Cited by 91
Ichikawa, H., & Sakata, T. (1998) · Journal of Nutrition · doi:10.1093/jn/128.5.843 · Cited by 90
The large intestine in nutrition and disease.
Cummings, J. H. (1997) · Cited by 89
Toden, S., Bird, A. R., Topping, D. L., & Conlon, M. A. (2007) · Cancer Biology & Therapy · doi:10.4161/cbt.6.2.3627 · Cited by 88
Preter, V. D., Geboes, K. P., Verbrugghe, K., Vuyst, L. D., Vanhoutte, T., Huys, G. R. B., Swings, J., Pot, B., & Verbeke, K. (2004) · British Journal Of Nutrition · doi:10.1079/bjn20041228 · Cited by 83
Self-citationPhenol Toxicity and Conjugation in Human Colonic Epithelial Cells
Pedersen, G., Brynskov, J., & Særmark, T. (2002) · Scandinavian Journal of Gastroenterology · doi:10.1080/003655202753387392 · Cited by 78
Matsumoto, M., & Benno, Y. (2004) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2004.07.016 · Cited by 75
Toden, S., Bird, A. R., Topping, D. L., & Conlon, M. A. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507336817 · Cited by 73
Hosoda, M., Hashimoto, H., He, F., Morita, H., & Hosono, A. (1996) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(96)76421-4 · Cited by 70
Glei, M., Haber, J. E., Oßwald, K., Seidel, C., Persin, C., Jahreis, G., & Pool-Zobel, B. (2005) · Biomarkers · doi:10.1080/13547500500138963 · Cited by 67
Impact of LKM512 yogurt on improvement of intestinal environment of the elderly
Matsumoto, M., Ohishi, H., & Benno, Y. (2001) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2001.tb00518.x · Cited by 66
Geboes, K., Hertogh, G. D., Preter, V. D., Luypaerts, A., Bammens, B., Evenepoel, P., Ghoos, Y. F., Geboes, K. J., Rutgeerts, P. J., & Verbeke, K. (2006) · British Journal Of Nutrition · doi:10.1017/bjn20061936 · Cited by 65
Self-citationThe Large Intestine in Nutrition and Disease
Heaton, K. W. (1997) · Journal of the Royal Society of Medicine · doi:10.1177/014107689709000715 · Cited by 64
Ndagijimana, M., Laghi, L., Vitali, B., Placucci, G., Brigidi, P., & Guerzoni, M. E. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.04.016 · Cited by 64
Preter, V. D., Vanhoutte, T., Huys, G. R. B., Swings, J., Rutgeerts, P., & Verbeke, K. (2006) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2006.02834.x · Cited by 61
Self-citationAlteration of Sulfate and Hydrogen Metabolism in the Human Colon by Changing Intestinal Transit Rate
Lewis, S. J., & Cochrane, S. (2006) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2006.01020.x · Cited by 60
Younes, H., Demigné, C., Behr, S. R., & Rémésy, C. (1995) · Nutrition Research · doi:10.1016/0271-5317(95)00079-x · Cited by 59
Colonic protein fermentation and promotion of colon carcinogenesis by thermolyzed casein
Corpet, D. E., Yin, Y., Zhang, X., Rémésy, C., Stamp, D., Medline, A., Thompson, L. U., Bruce, W. R., & Archer, M. C. (1995) · Nutrition and Cancer · doi:10.1080/01635589509514381 · Cited by 57
Sabatini, N., Perri, E., & Marsilio, V. (2009) · Innovative Food Science & Emerging Technologies · doi:10.1016/j.ifset.2009.05.001 · Cited by 53
Inter- and intra-individual variation of faecal water — genotoxicity in human colon cells
Oßwald, K., Becker, T. W., Grimm, M., Jahreis, G., & Pool-Zobel, B. L. (2000) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/s1383-5718(00)00113-3 · Cited by 50
Meat, starch, and nonstarch polysaccharides and large bowel cancer
Bingham, S. (1988) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/48.3.762 · Cited by 50
Preter, V. D., Coopmans, T., Rutgeerts, P. J., & Verbeke, K. (2006) · Journal of the American College of Nutrition · doi:10.1080/07315724.2006.10719570 · Cited by 47
Self-citationAssociations of Red Meat, Fat, and Protein Intake With Distal Colorectal Cancer Risk
Williams, C. D., Satia, J. A., Adair, L. S., Stevens, J., Galanko, J. A., Keku, T. O., & Sandler, R. S. (2010) · Nutrition and Cancer · doi:10.1080/01635581003605938 · Cited by 46
Heijnen, M. A., & Beynen, A. C. (1997) · Journal of Nutrition · doi:10.1093/jn/127.9.1828 · Cited by 43
Leschelle, X., Robert, V., Delpal, S., Mouillé, B., Mayeur, C., Latino‐Martel, P., & Blachier, F. (2002) · Cell Biology and Toxicology · doi:10.1023/a:1015515821390 · Cited by 42
Govers, M. J., Lapré, J. A., de Vries, H. T., & van der Meer, R. (1993) · Journal of Nutrition · doi:10.1093/jn/123.10.1709 · Cited by 40
Preter, V. D., Ghebretinsae, A. H., Abrahantes, J. C., Windey, K., Rutgeerts, P. J., & Verbeke, K. (2011) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201000442 · Cited by 26
Self-citationCross, A. J., Greetham, H. L., Pollock, J. R. A., Rowland, I. R., & Bingham, S. A. (2005) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20181 · Cited by 25
Synthesis of macromolecules by intestinal cells incubated with ammonia.
Topping, D. C., & Visek, W. (1977) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1977.233.4.e341 · Cited by 23
Benassi-Evans, B., Clifton, P. M., Noakes, M., & Fenech, M. F. (2010) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2010.08.009 · Cited by 19
Vis, E. H., Geerse, G.-J., Klaassens, E. S., van Boekel, M. A. J. S., & Alink, G. M. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5101_6 · Cited by 19
Moore, J. W. E., Millard, S. M., Babidge, W., Rowland, R., & Roediger, W. E. W. (1997) · Australian and New Zealand Journal of Surgery · doi:10.1111/j.1445-2197.1997.tb01956.x · Cited by 19
Fermentation of starch and protein in the colon: Implications for genomic instability
Leu, R. K. L., & Young, G. P. (2007) · Cancer Biology & Therapy · doi:10.4161/cbt.6.2.4078 · Cited by 17
Potential Protective Effects of Probiotics and Prebiotics Against Colorectal Cancer
Allsopp, P. J., & Rowland, I. R. (2009) · Springer eBooks · doi:10.1007/978-0-387-79058-9_26 · Cited by 12
Yagasaki, K. (2007) · Annals of Nutrition and Metabolism · Cited by 2
Research works printed but not linked: 1
- Benassi B., 2007, High protein‐high red meat and high carbohydrate weight loss diets do not differ in their effect on lymphocyte DNA damage using the cytokinesis‐block micronucleus cytome assay, Ann. Nutr. Metab., 51, 245
Cited by
Sorted by citations
The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication
Silva, Y. P., Bernardi, A., & Frozza, R. L. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00025 · Cited by 3,043
“Protein fermentation usually takes place in the distal large intestine where carbohydrates are already depleted and also leads to the production of potentially toxic metabolites, such as ammonia, phenols, and sulfides, as well as unique branched-chain fatty acids (BCFA) (69, 71).”
BackgroundThe gut microbiota, bacterial metabolites and colorectal cancer
Louis, P., Hold, G. L., & Flint, H. J. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3344 · Cited by 2,925
The impact of dietary fiber on gut microbiota in host health and disease
Makki, K., Deehan, E. C., Walter, J., & Bäckhed, F. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.05.012 · Cited by 2,517
The gut microbiota and host health: a new clinical frontier
Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., Hirschfield, G. M., Hold, G., Quraishi, M. N., Kinross, J., Smidt, H., Tuohy, K. M., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309990 · Cited by 2,302
“15 On the contrary, dietary fi bre or intake of plant-based foods appears to inhibit this, highlighting the importance of maintaining gut microbiome carbohydrate fermentation.”
BackgroundShort-chain fatty acids in control of body weight and insulin sensitivity
Canfora, E. E., Jocken, J. W., & Blaak, E. E. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.128 · Cited by 2,298
Metadata
- Authors
- Windey, K., De Preter, V., & Verbeke, K.
- Affiliations
- Universitair Ziekenhuis Leuven (BE)
- Corresponding author
- Verbeke, Kristin
- ORCID
- Verbeke, Kristin
- Venue
- Molecular Nutrition & Food Research
- Publisher
- Wiley
- Published
- 2011-11-25
- Volume
- 56
- Issue
- 1
- Pages
- 184-196
- ISSN
- 1613-4125 (ISSN-L)
- 1613-4133
- OpenAlex
- W2101238009
- Cited by
- 692
- References
- 106
- Citations by year
- 2026: 57 · 2025: 56 · 2024: 59 · 2023: 70 · 2022: 60 · 2021: 59 · 2020: 75 · 2019: 52 · 2018: 53 · 2017: 40 · 2016: 41 · 2015: 26 · 2014: 19 · 2013: 18 · 2012: 6
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Nutrition & Food Research (publishedVersion)
- PubMed (publishedVersion)
- Lirias (KU Leuven) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Keywords
- protein fermentation, gut health, distal colon, short-chain fatty acids, ammonia, amines, phenols, sulfide, colorectal cancer, ulcerative colitis, meat consumption, heme, heterocyclic amines, dietary fat, colonic metabolites
- MeSH terms
- Ammonia, Animals, Colon, Cresols, Diet, Fermentation, Humans, Hydrogen Sulfide, Meat, Phenols, Proteins, Colorectal Neoplasms, Gastrointestinal Tract
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