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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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
Flagged first, then by citations
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
Items 401–500 of 690
Microbiota regulation in constipation and colorectal cancer
Wang, L., Ruan, H., Wang, B., Qin, Y., & Zhong, W. (2023) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v15.i5.776 · Cited by 11
Indole signaling, a promising target to control vibriosis in aquaculture
Defoirdt, T. (2023) · Aquaculture · doi:10.1016/j.aquaculture.2023.739692 · Cited by 11
The Microbiome in Visceral Medicine: Inflammatory Bowel Disease, Obesity and Beyond
Chiriac, M. T., Mahapatro, M., Neurath, M. F., & Becker, C. (2017) · Visceral Medicine · doi:10.1159/000470892 · Cited by 11
Kamal, M., Cao, Y., Gao, J., Li, N., Zhao, X., Chen, L., Zhang, J., & Cheng, Y. (2025) · Animal Advances · doi:10.48130/animadv-0025-0008 · Cited by 11
Wang, X., Du, R., Liu, Y., Wang, L., & Wang, L. (2025) · Food Chemistry X · doi:10.1016/j.fochx.2025.102573 · Cited by 10
“Enhanced protein digestibility facilitates the release of amino acids, whereas reduced digestibility increases the presence of undigested proteins, leading to fermentation in the colon and elevating the risk of intestinal diseases (Windey et al., 2012).”
Precision nutrition for obesity management: A gut microbiota–centered weight-loss approach
Carvalho, L. M., da Mota, J. C. N. L., Ribeiro, A., Carvalho, B. G., Martínez, J. A., & Nicoletti, C. F. (2025) · Nutrition · doi:10.1016/j.nut.2025.112892 · Cited by 10
Sirven, M. A., Venâncio, V. P., Shankar, S., Klemashevich, C. L., Chicas, M. C., Fang, C., Mertens‐Talcott, S. U., & Talcott, S. T. (2021) · Food & Function · doi:10.1039/d1fo03047g · Cited by 11
Bachanek, I., Barszcz, M., Taciak, M., Tuśnio, A., & Skomiał, J. (2016) · Annals of Animal Science · doi:10.1515/aoas-2016-0043 · Cited by 10
Baliou, S., Adamaki, M., Spandidos, D. A., Kyriakopoulos, A. M., Christodoulou, I., & Zoumpourlis, V. C. (2018) · World Academy of Sciences Journal · doi:10.3892/wasj.2018.6 · Cited by 11
González‐Ortiz, G., Lee, S. A., Vienola, K., Raatikainen, K., Jurgens, G., Apajalahti, J., & Bedford, M. R. (2021) · Animal nutrition · doi:10.1016/j.aninu.2021.06.005 · Cited by 10
Maryati, Y., Nuraida, L., & Hariyadi, R. D. (2021) · Jurnal Kimia Sains dan Aplikasi · doi:10.14710/jksa.24.6.213-221 · Cited by 10
“Protein metabolism leads to the production of toxic and potentially carcinogenic compounds (such as ammonia or phenolic compounds) [18].”
BackgroundAcharya, S., & Thirunavukkarasu, C. (2024) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2902067 · Cited by 10
“Am-monia, phenols, nitrosamines, sulfides, etc are generated via protein fermentation by microbes mainly in the distal colon which are toxic and potential carcinogens [122].”
BackgroundBayona, C., Wrona, M., Ranđelović, T., Nerı́n, C., Salafranca, J., & Ochoa, I. (2024) · Biofabrication · doi:10.1088/1758-5090/ad5764 · Cited by 9
“Phenolic compounds are known break-down products of tyrosine through the process of proteolytic fermentation [34].”
Kaewsaen, R., Wichienchot, S., Thayanukul, P., Charoensiddhi, S., & Chanput, W. P. (2024) · Nutrients · doi:10.3390/nu16152553 · Cited by 9
“These compounds are produced through microbial metabolism of the aromatic amino acid tyrosine in the colon [45], which is associated with bowel diseases and the consumption of meat protein [46].”
BackgroundShah, T., Guo, X., Song, Y., Fang, Y., & Ding, L. (2024) · Animals · doi:10.3390/ani14162380 · Cited by 9
Impact of in ovo administration of xylo- and mannooligosaccharides on broiler chicken gut health
Bełdowska, A., Siwek, M. Z., Biesek, J., Barszcz, M., Tuśnio, A., Gawin, K., & Dunisławska, A. (2024) · Poultry Science · doi:10.1016/j.psj.2024.104261 · Cited by 9
“The results may suggest that this oligosaccharide has a potential to intensify deamination of amino acids or degradation of blood urea as these reactions lead to ammonia release (Windey et al., 2012).”
BackgroundMoretton, M., Casertano, M., Pellegrini, N., Anese, M., Fogliano, V., & Capuano, E. (2024) · Food & Function · doi:10.1039/d4fo02767a · Cited by 9
Zwolschen, J. W., Vos, A. P., Ariëns, R. M. C., & Schols, H. A. (2025) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2025.123352 · Cited by 9
Understanding how foods and enteral feedings influence the gut microbiome
Cresci, G. (2025) · Nutrition in Clinical Practice · doi:10.1002/ncp.11285 · Cited by 9
Enzymes and Gut Health in Monogastric Animals: Effects Beyond Digestibility
Pont, G. C. D., Eyng, C., Bortoluzzi, C., & Kogut, M. H. (2022) · The microbiomes of humans, animals, plants, and the environment · doi:10.1007/978-3-030-90303-9_3 · Cited by 10
Cordeiro, L., Cabrita, A. R. J., Oliveira, H. M., Maia, M. R. G., Rodrigues, J. A., Fonseca, A. J. M., & Valente, I. M. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c06662 · Cited by 9
Murray, M., Barlow, C. K., Blundell, S. A., Bücking, M., Gibbon, A., Göckener, B., Kaminskas, L. M., Leitner, P., Selby-Pham, S. N. B., Sinclair, A. J., et al. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1127729 · Cited by 10
Shi, A., Dong, L., Wu, Y., Liu, X., Li, W., Wang, J., Ji, X., Lv, H., Zhang, Y., & Wang, S. (2023) · Journal of Functional Foods · doi:10.1016/j.jff.2023.105690 · Cited by 9
The core components of cardio-oncology rehabilitation
Venturini, E., Gilchrist, S. C., Corsi, E., Lorenzo, A. D., Cuomo, G., D’AMBROSIO, G., Pacileo, M., D’Andrea, A., Canale, M. L., Iannuzzo, G., et al. (2021) · Panminerva Medica · doi:10.23736/s0031-0808.21.04303-2 · Cited by 9
Mehta, S., Dugas, L. R., Choo-Kang, C., Bovet, P., Forrester, T., Bedu-Addo, K., Lambert, E. V., Plange‐Rhule, J., Riesen, W., Korte, W. C., et al. (2021) · Nutrients · doi:10.3390/nu13072442 · Cited by 8
“However, high fiber diets can counteract these inflammatory and neoplastic pathways [48].”
BackgroundSchlörmann, W., Bockwoldt, J. A., Mayr, M. F., Lorkowski, S., Dawczynski, C., Rohn, S., Ehrmann, M. A., & Glei, M. (2021) · Food & Function · doi:10.1039/d1fo02175c · Cited by 10
Elastomer-coated graphene biosensor and its response to enzymatic reactions
Ono, T., Kannaka, M., Kanai, Y., Miyakawa, N., Shinagawa, A., Nakakita, S., Watanabe, Y., Ushiba, S., Tani, S., Suzuki, Y., et al. (2023) · Japanese Journal of Applied Physics · doi:10.35848/1347-4065/acda00 · Cited by 9
Understanding the microbiome: a primer on the role of the microbiome in colorectal neoplasia
Watson, K. M. (2020) · Annals of Gastroenterology · doi:10.20524/aog.2020.0467 · Cited by 9
“Ammonia is another product of protein fermentation, and has been well demonstrated to be carcinogenic at concentrations seen in western diets [107-109].”
BackgroundModulation of Gut Microbial Biomarkers and Metabolites in Cancer Management by Tea Compounds
Leung, H. K. M., Lo, E. K. K., Zhang, F., Felicianna, Ismaiah, M. J., Chen, C., & El-Nezami, H. S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126348 · Cited by 9
Microbial tryptophan catabolism as an actionable target via diet-microbiome interactions
Huang, Z., Wells, J. M., Fogliano, V., & Capuano, E. (2024) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2024.2369947 · Cited by 9
Bertarini, L., Imbeni, F., Brighenti, V., Martusciello, I., Pellati, F., & Alboni, S. (2025) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.5c00289 · Cited by 8
Effect of indigestible dietary protein on growth performance and health status of weaned pigs
Erinle, T. J., de Oliveira, M. J. K., Htoo, J. K. K., Mendoza, S. M., & Columbus, D. A. (2025) · Journal of Animal Science · doi:10.1093/jas/skaf372 · Cited by 8
Zhao, F., Wang, C., Song, S., Fang, C., Kristiansen, K., & Li, C. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202101124 · Cited by 11
Panah, F. M., Nielsen, K. D., Simpson, G. L., Schönherz, A. A., Schramm, A., Lauridsen, C., Nielsen, T. S., Højberg, O., Fredborg, M., Purup, S., et al. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1018242 · Cited by 9
“, biogenic amines, NH4, indoles, phenols, and H2S, are considered detrimental for gut health as they are capable of stimulating the immune system and starting a cascade of inflammatory responses in the colon (Windey et al., 2012; Gilbert et al., 2018; Panah et al., 2021).”
BackgroundKusumah, J., Castañeda-Reyes, E. D., Bringe, N. A., & de Mejı́a, E. G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512396 · Cited by 8
de Oliveira, L. I. G., Clementino, J. R., Salgaço, M. K., de Oliveira, S. P. A., Lima, M. D. S., Mesa, V., de Souza, E. L., Vinderola, C. G., Magnani, M., & Sivieri, K. (2023) · Food & Function · doi:10.1039/d3fo01156a · Cited by 8
Lammers-Jannink, K., Pellikaan, W. F., de Vries, S., Stigter, E. C. A., & Gerrits, W. J. J. (2023) · animal · doi:10.1016/j.animal.2023.101026 · Cited by 8
Dietary proteins: from evolution to engineering
Daniel, H. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1366174 · Cited by 9
“Amino acid oxidation leaves nitrogen and sulphur for detoxification which also results in a substantial flux of these entities through the large intestine with effects on the microbiome and not yet adequately defined health consequences (16, 17).”
BackgroundImpact of Nutrition on the Gut Microbiota
Ishiguro, E. E., Haskey, N., & Campbell, K. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-810541-2.00006-3 · Cited by 8
Rovalino-Córdova, A. M., Fogliano, V., & Capuano, E. (2021) · Food & Function · doi:10.1039/d1fo00321f · Cited by 8
Chen, J., Jing, H., Liu, H., Zhu, X., & Yang, G. (2023) · Animal Bioscience · doi:10.5713/ab.22.0060 · Cited by 8
“When the level of dietary protein is greater, there are increases in the populations of pathogens, such as Coliforms , Streptococcus and Bacillus [32].”
BackgroundKOROTKEVITCH, O. S., Эйзенах, И. А., Мозес, В. Г., & Захаров, И. С. (2018) · Fundamental and Clinical Medicine · doi:10.23946/2500-0764-2018-3-4-32-38 · Cited by 8
Andriamihaja, M., & Blachier, F. (2024) · Exploration of Medicine · doi:10.37349/emed.2024.00220 · Cited by 7
Behounek, M., Cochran, D., Romero, H. M., Yang, Q., Ding, W. R., Morton, M., Majumder, K., Powers, R., & Rose, D. J. (2024) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202300555 · Cited by 8
Ma, X., Fan, M., Hannachi, K., Qian, H., Li, Y., & Li, Y. (2024) · Food Research International · doi:10.1016/j.foodres.2024.115381 · Cited by 9
Liu, Y., Cao, L., Yu, C., Zhou, Q., Li, H., Zhang, R., Tang, J., Zhang, Z., Luo, Z., Jiang, X., et al. (2025) · Frontiers in Veterinary Science · doi:10.3389/fvets.2025.1525354 · Cited by 7
“It should be noted that the undigested and unabsorbed proteins reach the hindgut and are fermented by the distal intestinal flora to generate toxic nitrogen metabolites, such as ammonia, amines, hydrogen sulfide, and N -nitroso compounds (5), increasing the risk of postweaning diarrhea in piglets.”
Das, M., Duodu, S. O., Santra, S., Lalsangi, S. B., Naduviledathu, A., Bharati, R., Das, S., & Banerjee, R. (2025) · Food biomacromolecules. · doi:10.1002/fob2.70007 · Cited by 7
Nina, N., Bressa, C., de Lucas, B., de la Torre, I. M., Jiménez‐Aspee, F., Schmeda‐Hirschmann, G., & Larrosa, M. (2025) · Food Chemistry · doi:10.1016/j.foodchem.2025.144669 · Cited by 7
How nutrient starvation impacts the gut microbiome
Estrela, S., Long, J. Z., & Huang, K. C. (2025) · Nature Microbiology · doi:10.1038/s41564-025-02139-9 · Cited by 11
“Diet-induced compositional changes can alter the ability of the host to digest fibre 77 , proteins 78 and plant compounds such as isoflavones 79 , which further modifies the nutrient landscape.”
Feng, C., He, Q., Kwok, L., & Sun, Z. (2026) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2026.105818 · Cited by 7
In vivo evaluation of an innovative synbiotics on stage IIIb-IV chronic kidney disease patients
Vacca, M., Celano, G., Calabrese, F. M., Rocchetti, M. T., Iacobellis, I., Serale, N., Calasso, M. P., Gesualdo, L., & Angelis, M. D. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1215836 · Cited by 8
“org increase the possibility to detect potential detrimental metabolites, as derived from the fermentation of amino acids (52).”
BackgroundThe role of gut-derived short-chain fatty acids in Parkinson's disease
Saadh, M. J., Mustafa, A. N., Mustafa, M. A., Renuka Jyothi, S., Dabis, H. K., Prasad, G. V. S., Mohammad, I. J., Adnan, A., & Idan, A. H. (2024) · Neurogenetics · doi:10.1007/s10048-024-00779-3 · Cited by 9
“Protein fermentation often occurs in the distal large intestine, when carbohydrates have already been eliminated, leading to the production of potentially harmful metabolites such as phenols, ammonia, and sulfides, as well as branched-chain fatty acids (BCFA) [36, 37].”
Zhong, Y., Liu, Z., Wang, Y., Cai, S., Qiao, Z., Hu, X., Wang, T., & Yi, J. (2024) · Food Reviews International · doi:10.1080/87559129.2024.2414908 · Cited by 11
“[59] Furthermore, reactive oxygen intermediates belong to a class of carcinogenic metabolites derived from gut microbiota.”
Han, B. R., Zhang, Y., Feng, X., Yang, J. J. J., Wang, B., Fang, J., Wang, Z., Zhu, J., Niu, G., & Guo, Y. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1563886 · Cited by 7
“Ammonia is also considered a potential carcinogen at low concentrations, with existing animal model studies demonstrating its association with intestinal mucosal damage and CRC development (113).”
Khemis, I. B., Knani, S., Aouaini, F., Graba, B. B., & Lamine, A. B. (2025) · Materials Chemistry and Physics · doi:10.1016/j.matchemphys.2025.130929 · Cited by 7
Lukichev, B. G., Rumyantsev, A. S., Panina, I. Y., & Акименко, В. Б. (2019) · Nephrology (Saint-Petersburg) · doi:10.24884/1561-6274-2018-23-1-18-31 · Cited by 9
“Ферментация белка из непереваренных или эндогенных источников белка в отсутствие сбраживаемых углеводов может привести к образованию и накоплению потенциально вредных метаболитов, таких как сульфиды, амины, аммиак и различные фенолы [27].”
INTERACTION BETWEEN FOOD PYRAMID AND GUT MICROBIOTA. A NEW NUTRITIONAL APPROACH
Magro, D. O., Rossoni, C., Saad-Hossne, R., & Santos, A. (2023) · Arquivos de Gastroenterologia · doi:10.1590/s0004-2803.202301000-15 · Cited by 7
Belloumi, D., Calvet, S., Roca, M., Ferrer, P., Jiménez-Belenguer, A. I., Cambra‐López, M., Garcia-Rebollar, P., Climent, E., Martínez-Blanch, J. F., Tortajada, M., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-44741-z · Cited by 7
“Protein fermentation (or putrefaction) is an anaerobic degradation of non-digested proteins and AA that escape the digestion in the small intestine by the anaerobic bacteria of the hindgut 50,51 .”
BackgroundGiromini, C., Baldi, A., Fusi, E., Rebucci, R., & Purup, S. (2015) · Cell Biology and Toxicology · doi:10.1007/s10565-015-9304-y · Cited by 7
“The microbial community of the human colon is responsible for the active breakdown of food, particularly carbohydrates and proteins that have escaped digestion in the small intestine (Windey et al 2012).”
Connolly, K. R., Sweeney, T., Ryan, M. T., Vigors, S., & O’Doherty, J. V. (2025) · Microorganisms · doi:10.3390/microorganisms13030689 · Cited by 6
“This fermentation produces toxic metabolites, reducing gastrointestinal structure and function and contributes to post-weaning diarrhoea (PWD) [3,6–8], which has traditionally been managed by adding zinc oxide to the diet.”
Sooraj, I. P., Leech, J., O’Callaghan, T. F., & McAuliffe, O. E. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1638378 · Cited by 7
“However, there is a lack of clarity on the effective toxicity of these compounds in humans, current understanding is based on animal and in vivo studies and these thresholds are not well established (Windey et al., 2012).”
InfluentialDing, W. R., Bai, Y., & Rose, D. J. (2025) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.70299 · Cited by 7
RETRACTED: Understanding microbiota-driven oncogenesis: The role of metabolites in tumorigenesis
Ullah, S., Wu, C., Zou, X., Zhong, Y., Ahmad, A., Jan, A. U., Cong, Y., Chen, Y., & Li, L. (2025) · iScience · doi:10.1016/j.isci.2025.113945 · Cited by 8
RetractedWu, W., Wang, S., Xue, C., & Dong, N. (2026) · Animal nutrition · doi:10.1016/j.aninu.2025.10.004 · Cited by 6
Kurmaev, D. P., Bulgakova, S. V., Treneva, E. V., Pervyshin, N. A., Sharonova, L. A., & Dolgikh, Y. A. (2024) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-222-2-111-119 · Cited by 6
Jangra, B., Kulshreshtha, S., Goyal, A., & Jachak, S. M. (2025) · Phytomedicine Plus · doi:10.1016/j.phyplu.2025.100731 · Cited by 6
Natural blue colourant preparations from blue pea flower and spirulina: A comparison stability study
Gamage, G. C. V., Goh, J. K., & Choo, W. S. (2023) · Food Chemistry Advances · doi:10.1016/j.focha.2023.100457 · Cited by 6
“Products such as ammonia, amines, cresol, indole, and phenols could be produced during protein breakdown (Windey, De Preter & Verbeke, 2012).”
BackgroundDietary Protein and Colonic Microbiota
Boudry, G., Le Huërou-Luron, I., & Michel, C. (2016) · The Molecular Nutrition of Amino Acids and Proteins · doi:10.1016/b978-0-12-802167-5.00015-3 · Cited by 5
Association between exercise and changes in gut microbiota profile: a review
Khaledi, M., Darvishi, M., Sameni, F., Shahrjerdi, S., Karami, E., Barahui, N., Hemmati, J., Hasheminasab, M. S., Sanae, M.-J., Akhavan‐Sigari, R., et al. (2023) · Sport Sciences for Health · doi:10.1007/s11332-023-01132-1 · Cited by 5
“High levels of H2S and urea in the gut have been observed in elite athletes due to pathobionts (i.e., Fusobacterium , Veil-lonella , and Atopobium parvulum ) and high-protein diets, which produce NO and deteriorate mitochondrial activity and cause bacterial infection [83, 84].”
Sarcopenic Obesity: The Underlying Molecular Pathophysiology and Prospect Therapies
Meiliana, A., Dewi, N. M., Defi, I. R., Rosdianto, A. M., Qiantori, A. A., & Wijaya, A. (2024) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v16i4.3176 · Cited by 4
“(122 ,126,127) Certain metabolic byproducts are harmful to metabolic health and have been linked to a number of disorders, including inflammatory bowel disease and colorectal cancer, as well as chronic inflammation.”
BackgroundLuévano, J. M., Liu, J. C., & Stappenbeck, T. S. (2025) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000864 · Cited by 6
“Protein fermentation di ff ers from saccharolytic fermentation in that it produces many similar SCFAs from a carbon skeleton, but also releases potentially toxic nitrogenous and sulfur metabolites such as ammonia, amines, nitrates, nitrites, and hydrogen sul fi de (129) (Figure 4).”
Wang, Z., Chen, G., Sun, X., Xiao, J., Kong, L., Jiang, S., Xu, T., Wang, M., & Zhao, H. (2025) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1644014 · Cited by 7
“In the distal colon under high-fat diet conditions—characterized by limited fermentable carbohydrates—gut microbiota preferentially engage in proteolytic metabolism, driving BCFAs overproduction (62).”
The fate of dietary protein in the gastrointestinal tract and implications for colonic disease
Davis, R. W., Bryant, R. V., Gibson, P. R., & Day, A. S. (2026) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-026-01173-0 · Cited by 6
Exploring the Role of Mentha in Gut Microbiota: A Modern Perspective of an Ancient Herb
Arora, S., & Sharma, A. K. (2023) · Recent Advances in Food Nutrition & Agriculture · doi:10.2174/2772574x14666230411101712 · Cited by 5
Chapman, J. A., Wroot, E., Brown, T., Beck, L. C., Embleton, N. D., Berrington, J. E., & Stewart, C. J. (2024) · BMC Microbiology · doi:10.1186/s12866-024-03701-x · Cited by 5
Kampf, G. (2018) · Fundamental and Clinical Medicine · doi:10.23946/2500-0764-2018-3-4-60-72 · Cited by 5
Dietary Proteins Alter Fermentation Characteristics of Human Gut Microbiota In Vitro
Xiao, T., Liang, T., Geng, D., Wang, L., Liu, L., Zhou, X., Pu, H., Huang, J., Zhou, S., & Tong, L. (2020) · Plant Foods for Human Nutrition · doi:10.1007/s11130-020-00836-w · Cited by 5
Ďásková, N., Heczková, M., Módos, I., Hradecký, J., Hudcovic, T., Kuzma, M., Pelantová, H., Buskova, I., Sticová, E., Funda, D. P., et al. (2023) · Nutrients · doi:10.3390/nu15020454 · Cited by 7
“Protein fermentation yields intrinsically toxic luminal compounds that affect epithelial cell metabolism and barrier function [58].”
BackgroundYu, X., Nie, W., Chen, X., Zou, L., Xu, B., & Chen, C. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.130246 · Cited by 5
Microbiota and detrimental protein derived metabolites in colorectal cancer
González, A., Odriozola, I., Fullaondo, A., & Odriozola, A. (2024) · Advances in genetics · doi:10.1016/bs.adgen.2024.06.001 · Cited by 7
Factors affecting plant food particle behaviour during in vitro colonic microbial fermentation
Yao, H. L., Flanagan, B. M., Williams, B. A., Mikkelsen, D., & Gidley, M. J. (2024) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2024.104802 · Cited by 5
Paturi, G., Bentley‐Hewitt, K. L., Butts, C. A., Nyanhanda, T., Monro, J. A., & Ansell, J. (2013) · International Journal of Food Science & Technology · doi:10.1111/ijfs.12208 · Cited by 5
“When diets high in protein are consumed, the distal colon microbiota utilise the accumulated protein as an alternative carbon source, which leads to the formation of potentially toxic compounds (Russell et al., 2011; Windey et al., 2012).”
BackgroundLe, M. H. A., Buchet, A. D. G., Beltranena, E., Gerrits, W. J. J., & Zijlstra, R. T. (2017) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2017.09.005 · Cited by 5
FOURTH UNIVERSAL DEFINITION OF MYOCARDIAL INFARCTION. FOCUS ON THE TYPE 2 MYOCARDIAL INFARCTION
Барбараш, О. Л., & Кашталап, В. В. (2018) · Fundamental and Clinical Medicine · doi:10.23946/2500-0764-2018-3-4-73-82 · Cited by 5
Effects of Different Ionic Polysaccharides in Cooked Lean Pork Batters on Intestinal Health in Mice
Yu, X., Zou, L., Xiong, J.-H., Pan, J.-Z., Li, P.-J., & Chen, C. (2022) · Foods · doi:10.3390/foods11101372 · Cited by 5
“In addition, undigested protein and/or unabsorbed amino acids pass into the colon and are subjected to anaerobic fermentation by gut microbes, thus impairing the host’s health [27].”
Backgroundvan Zanten, G. C., Madsen, A. L., Yde, C. C., Krych, Ł., Yeung, N., Saarinen, M., Kot, W., Jensen, H. M., Rasmussen, M. A., Ouwehand, A. C., et al. (2024) · Microorganisms · doi:10.3390/microorganisms12040796 · Cited by 6
“BCFAs are commonly used as biomarkers of colonic protein fermentation leading to the concomitant production of other potentially toxic protein fermentation products such as ammonia, phenol, and H 2 S, which can cause cell damage in the intestine [53,54].”
Background“We Are What We Eat”: How Diet Impacts the Gut Microbiota in Adulthood
Wang, T., Roest, D. I. M., Smidt, H., & Zoetendal, E. G. (2019) · Springer eBooks · doi:10.1007/978-3-030-28737-5_11 · Cited by 5
Which Microbes Like My Diet and What Does It Mean for My Heart?
Sawicka, E., Moniuszko-Malinowska, A. M., & Kamiński, K. A. (2021) · Nutrients · doi:10.3390/nu13114146 · Cited by 5
“The gut microbiome composition in animal models seems to be strictly associated with the consumption of dietary protein, whereby doses from 100 to 200 g/kg caused an increase in Lactobacilli and a reduction in Coliformis and Staphylococci; doses greater than 200 g/kg caused an increase in Coliforms, Streptococcus and…”
BackgroundInfluentialPhenylpropionc acid produced by gut microbiota alleviates acetaminophen-induced hepatotoxicityPreprint
Cho, S., Yang, X., Won, K., Leone, V., Hubert, N., Chang, E. B., Chung, E., Park, J., Guzman, G., Lee, H. W., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/811984 · Cited by 5
“A large portion of phenylalanine available to gut bacteria in the large intestine is derived from proteolytic degradation of proteins by gut bacteria, which releases free phenylalanine or phenylalanine-containing peptides (60).”
BackgroundCharacteristics of synbiotics and lactobionic acid
Goderska, K., & Obey, P. O. (2025) · Journal of Functional Foods · doi:10.1016/j.jff.2025.107058 · Cited by 4
Govindan, A., Du, H., Manjaly, J. P., Patangia, D. V., Zannini, E., Woods, T., Donoghue, D. O., Ross, R. P., & Stanton, C. (2025) · Food Nutrition · doi:10.1016/j.fnutr.2025.100050 · Cited by 5
Adejumo, S. A., Lewis, G., Das, P., Lim, C. K. Y., Malas, J., Oli, A. N., Allen, J. M., & Hampton‐Marcell, J. (2026) · Advances in Nutrition · doi:10.1016/j.advnut.2025.100582 · Cited by 6
Opperman, C., Lloyd, C., Ratanpaul, V., Van, T. T. H., Brennan, C. S., & Eri, R. D. (2026) · Food Research International · doi:10.1016/j.foodres.2026.118846 · Cited by 4
Vigneswaran, J., Keskey, R. C., Morgan, R. B., Alverdy, J. C., Alpert, L., Chang, E. B., Weichselbaum, R. R., Zaborina, O. Y., & Shogan, B. D. (2023) · Annals of Surgery · doi:10.1097/sla.0000000000006052 · Cited by 4
“36 This could exacerbate the proliferative migratory environment within the healing anastomotic tissue.”
BackgroundDetermination of the Impact of Extruded Soybean Press Cake on Rearing and Health Indices of Piglets
Świątkiewicz, M., Szczepanik, K., Gala, Ł., GRELA, E. R., Witaszek, K., Barszcz, M., Tuśnio, A., & Taciak, M. (2024) · Agriculture · doi:10.3390/agriculture14111899 · Cited by 4
Xie, Z., Eriksen, D. B., Johnsen, P. R., Nielsen, D. S., & Frøkiær, H. (2025) · BioFactors · doi:10.1002/biof.70007 · Cited by 4
“4,44,45 Notably, gut-derived metabolites enter systemic circulation, reaching distal organs and tissues where they can influence physiological processes and health.”
Xiong, W., Jama, H. A., Flanagan, B. M., Peh, A., Antonacci, S., Xu, C., Dhital, S., & Marques, F. Z. (2025) · Food Hydrocolloids · doi:10.1016/j.foodhyd.2025.111878 · Cited by 5
Huang, R., Yao, H. L., Ji, S.-Y., Wu, J., Lin, Q., Gupta, T. B., Gan, D., & Wu, X. (2024) · Food Bioscience · doi:10.1016/j.fbio.2024.104089 · Cited by 4
Niu, Y., Yu, H., Yan, Z.-H., & Yan, X. (2024) · Journal of Nutrition · doi:10.1016/j.tjnut.2024.04.033 · Cited by 4
de Oliveira, M. J. K., Babatunde, O. O., Rodrigues, L. A., Erinle, T. J., Htoo, J. K., Mendoza, S. M., & Columbus, D. A. (2024) · Journal of Animal Science · doi:10.1093/jas/skae374 · Cited by 6
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review