Gut microbiota metabolites, amino acid metabolites and improvements in insulin sensitivity and glucose metabolism: the POUNDS Lost trial
Open accessAbstract
Objective Alterations in gut microbiota have been linked to host insulin resistance, diabetes and impaired amino acid metabolism. We investigated whether changes in gut microbiota-dependent metabolite of trimethylamine N-oxide (TMAO) and its nutrient precursors (choline and L-carnitine) were associated with improvements in glucose metabolism and diabetes-related amino acids in a weight-loss diet intervention. Design We included 504 overweight and obese adults who were randomly assigned to one of four energy-reduced diets varying in macronutrient intake. The 6-month changes (Δ) in TMAO, choline and L-carnitine levels after the intervention were calculated. Results Greater decreases in choline and L-carnitine were significantly (p<0.05) associated with greater improvements in fasting insulin concentrations and homeostasis model assessment of insulin resistance (HOMA-IR) at 6 months. The reduction of choline was significantly related to 2-year improvements in glucose and insulin resistance. We found significant linkages between dietary fat intake and ΔTMAO for changes in fasting glucose, insulin and HOMA-IR (p interaction <0.05); a greater increase in TMAO was related to lesser improvements in the outcomes among participants who consumed a high-fat diet. In addition, ΔL-carnitine and Δcholine were significantly related to changes in amino acids (including branched-chain and aromatic amino acids). Interestingly, the associations of ΔTMAO, Δcholine and ΔL-carnitine with diabetes-related traits were independent of the changes in amino acids. Conclusion Our findings underscore the importance of changes in TMAO, choline and L-carnitine in improving insulin sensitivity during a weight-loss intervention for obese patients. Dietary fat intake may modify the associations of TMAO with insulin sensitivity and glucose metabolism. Trial registration number NCT00072995 .
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Changes in trimethylamine N-oxide and choline were associated with increased insulin sensitivity in a weight-loss intervention study of obese individuals.
“Changes in TMAO and choline associated with increased insulin sensitivity in a weight-loss intervention study of obese individuals.155”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [155]
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“These metabolites mainly include short ‐ chain fatty acids (SCFAs) [162], amino acid metabolites [163], vitamins [164], bile acids (BAs) [165], lactic acid [166], toxins [167], and formate [168], among others.”
BackgroundDiabetes and the Gut Microbiome
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“41 TMAO has been related to increased risk of T2DM in a cross-sectional study of the Chinese population 42 and in a meta-analysis of 12 clinical studies 40 ; however, null associations have been reported in one of two cohorts in another Chinese study 43 and a Norwegian study.”
Elevated plasma trimethylamine-N-oxide levels are associated with diabetic retinopathy
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“The levels of choline decreased with weight loss, consistent with previous reports associating this with improvements in insulin sensitivity [51] and a more favorable cardio-metabolic risk factor pattern in general [52].”
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Gut Microbiota-Derived Metabolites in the Development of Diseases
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Alzheimer’s disease and gut microbiota: does trimethylamine N-oxide (TMAO) play a role?
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Therapeutic potential of natural products against atherosclerosis: Targeting on gut microbiota
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A dynamics association study of gut barrier and microbiota in hyperuricemia
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“Advances in high-throughput sequencing have facilitated a comprehensive profiling of gut microbial compositions and their functional capacities in metabolic disease, including obesity, insulin resistance, and type 2 diabetes (Heianza et al., 2019; Wu H. et al., 2020; Choi and Yang-Jensen, 2023).”
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TMAO and diabetes: from the gut feeling to the heart of the problem
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“In contrast, a Western diet, rich in fats and meat, tends to increase this metabolite [106, 114, 115], although fi sh consumption was associated with signi fi cantly greater increases in circulating TMAO than consumption of eggs or beef [116].”
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“Gut microbiota promotes the energy metabolism, immunity, and brain health of the host via microbiota metabolites, such as amino acids and short-chain fatty acids (SCFAs) (Heianza et al., 2019; Li et al., 2019).”
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“These changes may lead to increased levels of adiposity and impaired insulin signaling [15,17,18].”
BackgroundBone Homeostasis and Gut Microbial-Dependent Signaling Pathways
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“Most studies reported that carnitine was associated with the development and progress of diabetes mellitus for multiperspectives such as microbiota [38] and lipid [39].”
BackgroundNitrated fatty acids: from diet to disease
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“TMAO is an important secondary metabolite produced by the gut microbiota that can change insulin sensitivity and blood sugar levels, even with subtle alterations [86].”
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Gut microbiota in surgical and critically ill patients
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Diets, Gut Microbiota and Metabolites
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“TMA can be further oxidized to trimethylamine N-oxide, which could trigger insulin resistance and increase the risk of T2DM and NAFLD in humans and rodents (Barrea et al. 2018; Fu et al. 2020; Heianza et al. 2019; Schugar et al. 2017; Shan et al. 2017).”
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Amino Acid-Induced Impairment of Insulin Signaling and Involvement of G-Protein Coupling Receptor
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Nutrition for precision health: The time is now
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Self-citationBibliometric visualization analysis of gut-kidney axis from 2003 to 2022
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“Participants with lowered TMAO showed a decrease in fasting blood glucose and a significant increase in insulin sensitivity, while participants with elevated TMAO showed a smaller improvement in fasting blood glucose and insulin sensitivity, providing strong evidence of the important role of TMAO in the development of…”
BackgroundGut microbiota: an emerging target connecting polycystic ovarian syndrome and insulin resistance
Mei, Y., Li, W., Wang, B., Chen, Z., Wu, X., Lin, Y., & Wang, M. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1508893 · Cited by 27 · see citing works
“In fact, elevated TMAO is directly associated with increased IR risk; dietary interventions or targeting gut microbiota can effectively reduce blood levels of TMAO and its precursors, improving fasting glucose and HOMA-IR (Heianza et al., 2019).”
InfluentialLiu, J., Li, F., Yang, L., Luo, S., & Deng, Y. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1554189 · Cited by 26 · see citing works
Dysbiosis of Gut Microbiota Contributes to the Development of Diabetes Mellitus
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Type 2 Diabetes Remission 5 Years After Laparoscopic Sleeve Gastrectomy: Multicenter Cohort Study
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Host genetics and gut microbiota jointly regulate blood biochemical indicators in chickens
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“Furthermore, the gut microbiota is capable of regulating numerous metabolic processes in the host, including energy homeostasis, glucose metabolism (Karls-son et al. 2013; Heianza et al. 2019), and lipid metabolism (Hu et al. 2022).”
BackgroundSelf-citationGut Microbe-Generated Metabolite Trimethylamine-N-Oxide and Ischemic Stroke
Li, Z., He, X., Fang, Q., & Yin, X. (2024) · Biomolecules · doi:10.3390/biom14111463 · Cited by 26 · see citing works
“In overweight individuals who participated in a dietary intervention, reduced circulating TMAO levels were associated with improved insulin sensitivity [48].”
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Zhou, W., Han, L., Raza, S. H. A., Yue, Q., Sun, S., Zhao, Y., Lv, L., Deng, Y., Yuan, Z., Alsharif, I., et al. (2022) · Journal of Functional Foods · doi:10.1016/j.jff.2022.105381 · Cited by 24 · see citing works
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“Additional microbial metabolites like succinate and trimethylamine n-oxide (TMAO) affect glucose metabolism [56, 57].”
Zhang, G., Ma, F., Zhang, Z., Qi, Z., Luo, M., & Yu, Y. (2023) · Environment International · doi:10.1016/j.envint.2023.107802 · Cited by 23 · see citing works
Xu, N., Wan, J., Wang, C., Liu, J., Qian, C., & Tan, H. (2022) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s370206 · Cited by 22 · see citing works
“A high TMAO level could reduce glucose homeostasis consequences to the worst clinical result of diabetic complications.(16,17) Thus, TMAO probably plays a significant role that was previously unrecognized in T2DMassociated cognitive impairment.”
BackgroundIntestinal Translocation of Live Porphyromonas gingivalis Drives Insulin Resistance
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“Regarded as the second human genome, the roles of gut microbiota and their metabolites in the regulation of insulin resistance have received increasing attention (Brial et al. 2018; Heianza et al. 2019).”
BackgroundNon-antibiotic therapy forClostridioides difficileinfection: a review
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Gut microbiota: A potential therapeutic target for management of diabetic retinopathy?
Yempén, R. E. A., Venzel, R., Campos, M. C. P., de Oliveira, L. P., Lins, R. V. D., Pessoni, A. M., Fanaro, G. B., Souza, A. D. O., Calaza, K. D. C., Alves, J. L. D. B., et al. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.120060 · Cited by 22 · see citing works
Jiang, W., Huo, J.-Y., Wang, S.-C., Cheng, Y.-D., Lyu, Y.-T., Jiang, Z., & Shan, Q. (2022) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-022-00908-2 · Cited by 21 · see citing works
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“A cohort study demonstrated a weak but significant correlation between the decreased TMAO levels and alleviation of IR [84].”
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Toward Precision Weight-Loss Dietary Interventions: Findings from the POUNDS Lost Trial
Qi, L., Heianza, Y., Li, X., Sacks, F. M., & Bray, G. A. (2023) · Nutrients · doi:10.3390/nu15163665 · Cited by 17 · see citing works
“These suggested that the observed results are possibly through different pathways or mechanisms related to diabetes-related amino acids [91], and the independent roles of the TMAO-related metabolism in regulating the metabolic responses to weight-loss diet interventions.”
Self-citationPapandreou, C., Harrold, J. A., Hansen, T. T., Halford, J. C. G., Sjödin, A. M., & Bulló, M. (2021) · Nutrients · doi:10.3390/nu13124289 · Cited by 17 · see citing works
“A more recent study nested within the POUNDS lost trial demonstrated that reductions in plasma choline and trimethylamine N-oxide were associated with improvements in insulin sensitivity after 6months of LCD [8].”
ResultDHA Suppresses Hepatic Lipid Accumulation via Cyclin D1 in Zebrafish
Ding, Q., Hao, Q., Zhang, Q., Yang, Y., Olsen, R. E., Ringø, E., Ran, C., Zhang, Z., & Zhou, Z. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2021.797510 · Cited by 17 · see citing works
Liu, P., Li, H., Xu, H., Gong, J., Jiang, M., Xu, Z., & Shi, J. (2023) · iScience · doi:10.1016/j.isci.2023.107754 · Cited by 17 · see citing works
- Authors
- Heianza, Y., Sun, D., Li, X., DiDonato, J. A., Bray, G. A., Sacks, F. M., & Qi, L.
- Affiliations
- Tulane University (US)
- Cleveland Clinic (US)
- Pennington Biomedical Research Center (US)
- Harvard University (US)
- Corresponding author
- Qi, Lu
- Venue
- Gut
- Publisher
- BMJ
- Published
- 2018-06-02
- Volume
- 68
- Issue
- 2
- Pages
- 263-270
- ISSN
- 0017-5749 (ISSN-L)
- 1468-3288
- PMC
- PMC6275143
- OpenAlex
- W2806227292
- Cited by
- 177
- References
- 52
- Citations by year
- 2026: 10 · 2025: 25 · 2024: 22 · 2023: 22 · 2022: 25 · 2021: 32 · 2020: 18 · 2019: 16 · 2018: 6
- FWCI
- 6.40
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Gut (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Heart, Lung, and Blood Institute
- Japan Society for the Promotion of Science
- United States-Israel Binational Science Foundation
- National Institute of Diabetes and Digestive and Kidney Diseases
- Boston Obesity Nutrition Research Center
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- gut microbiota metabolites, trimethylamine N-oxide, choline, L-carnitine, insulin resistance, insulin sensitivity, glucose metabolism, weight loss diet, macronutrient composition, dietary fat intake, branched-chain amino acids, aromatic amino acids, obesity, POUNDS Lost trial
- MeSH terms
- Gastrointestinal Microbiome, Adult, Amino Acids, Carnitine, Choline, Diet, Reducing, Female, Glucose, Humans, Insulin Resistance, Male, Massachusetts, Methylamines, Obesity, Overweight
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