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Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women
Open accessAbstract
AIMS: Carnitine and choline are major nutrient precursors for gut microbiota-dependent generation of the atherogenic metabolite, trimethylamine N-oxide (TMAO). We performed randomized-controlled dietary intervention studies to explore the impact of chronic dietary patterns on TMAO levels, metabolism and renal excretion. METHODS AND RESULTS: Volunteers (N = 113) were enrolled in a randomized 2-arm (high- or low-saturated fat) crossover design study. Within each arm, three 4-week isocaloric diets (with washout period between each) were evaluated (all meals prepared in metabolic kitchen with 25% calories from protein) to examine the effects of red meat, white meat, or non-meat protein on TMAO metabolism. Trimethylamine N-oxide and other trimethylamine (TMA) related metabolites were quantified at the end of each diet period. A random subset (N = 13) of subjects also participated in heavy isotope tracer studies. Chronic red meat, but not white meat or non-meat ingestion, increased plasma and urine TMAO (each >two-fold; P < 0.0001). Red meat ingestion also significantly reduced fractional renal excretion of TMAO (P < 0.05), but conversely, increased fractional renal excretion of carnitine, and two alternative gut microbiota-generated metabolites of carnitine, γ-butyrobetaine, and crotonobetaine (P < 0.05). Oral isotope challenge revealed red meat or white meat (vs. non-meat) increased TMA and TMAO production from carnitine (P < 0.05 each) but not choline. Dietary-saturated fat failed to impact TMAO or its metabolites. CONCLUSION: Chronic dietary red meat increases systemic TMAO levels through: (i) enhanced dietary precursors; (ii) increased microbial TMA/TMAO production from carnitine, but not choline; and (iii) reduced renal TMAO excretion. Discontinuation of dietary red meat reduces plasma TMAO within 4 weeks.
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32 Own result · 21 Not checked yet · 8 Own interpretation · 6 Own method · 2 Partly supported · 1 Supported so far · accuracy not yet measured
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In the paper
“Interestingly, in small cross-sectional observational studies, plasma levels of TMAO were modestly increased in omnivores relative to vegans/vegetarians, and in recent clinical challenge studies, TMA and TMAO generation from oral carnitine was observed to be substantially reduced in vegans/vegetarians.3,19”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Partly supportedcites [3] Koeth, 2013, Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis, Nat Med sourceExperimental — accuracy not yet measured
The Results section, “Vegans and vegetarians produce less TMAO from L-carnitine” (page unavailable), reports markedly reduced TMAO production after an oral carnitine challenge in long-term vegans/vegetarians. It does not report a corresponding reduction in TMA generation in those human participants; the passages reporting TMA measurements concern mice. (LLM, conf=0.85)
- Supportedcites [19] Koeth, 2018, L-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans, J Clin Invest source
The clinical challenge results report minimal TMAO production from oral carnitine in vegans/vegetarians at baseline, while omnivores readily produced it. The paper also reports greater microbial conversion to TMA in omnivores. Supplementation increased TMAO production in some vegans/vegetarians, but the Discussion says their production capacity remained lower overall. Page numbers were not supplied in the passages. (LLM, conf=0.93)
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In the paper
“In contrast, the fractional renal excretion of carnitine, c-butyrobetaine, and crotonobetaine increased significantly (P < 0.0001, P < 0.0001, and P = 0.0007, respectively) on the red meat diet in comparison to the non-meat diet (Figure 5D-F).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
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In the paper
“Interestingly, very modest but statistically significant reductions were noted in plasma betaine and urine choline concentrations following chronic consumption of the red meat diet compared with the non-meat or white meat diets (Figures 2A and 3).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Two additional carnitine related metabolites generated by gut microbiota, c-butyrobetaine, and crotonobetaine, 16,19 both showed significant increases in both plasma (P < 0.0001 and P = 0.004, respectively) and urine (P < 0.0001 each) concentrations following 4 weeks of the red meat diet, though the relative magnitude of the increase was smaller than that for TMAO (Figures 2A and 3).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Two additional carnitine related metabolites generated by gut microbiota, c-butyrobetaine, and crotonobetaine, 16,19 both showed significant increases in both plasma (P < 0.0001 and P = 0.004, respectively) and urine (P < 0.0001 each) concentrations following 4 weeks of the red meat diet, though the relative magnitude of the increase was smaller than that for TMAO (Figures 2A and 3).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Notably, plasma levels of TMAO were most strongly correlated to choline and carnitine (and choline and carnitine with one another), particularly following 4 weeks of the red meat and white meat diets.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Thus, increased level of dietary-saturated fat had no effect on plasma concentrations of TMAO.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Further, we too had performed unpublished untargeted metabolomics analyses and identified symmetric dimethylarginine (SDMA) as being highly correlated with renal function (r > 0.80; P < 0.0001) in both men and women alike (data not shown), and alternative published studies have similarly suggested SDMA serves as an excellent endogenous marker of renal function. 25”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
What the sources say
- Not checked yetcites [25] Kielstein, 2006, Symmetric dimethylarginine (SDMA) as endogenous marker of renal function–a meta-analysis, Nephrol Dial Transplant source
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In the paper
“For example, the 24 h urine d3-TMA and d3-TMAO recovered following ingestion of d3-carnitine was significantly (several-fold) higher in subjects following either the red meat or white meat diets compared to the non-meat diet (Figure 7A and B).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
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In the paper
“Plasma levels of each of the monitored metabolites following 4 weeks of low-vs.high-saturated fat diets failed to show any significant differences (Figure 4A).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Similarly, the 24 h urine d3-carnitine, d3-c-butyrobetaine, and d3-crotonobetaine were all significantly increased in subjects following the red meat diet (Figure 7C-E).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
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In the paper
“Similarly, 24 h urinary total d6-choline and d6betaine recovered following each diet intervention showed no significant differences, except for a modest decrease following 4 weeks of white meat diet vs. red meat (Figure 6C and D).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
plainn = 13- Asserted: passes — The authors put it forward as true.
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In the paper
“Remarkably, 24 h urine choline-derived d6-TMA and d6-TMAO showed no significant differences within subjects following the month long exposures to each of the distinct diets (Figure 6A and B).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
plainn = 13- Asserted: passes — The authors put it forward as true.
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In the paper
“Moreover, when subjects discontinued the red meat diet and moved to either the white meat or non-meat diet, a marked reduction in fasting plasma TMAO level was observed (Figure 2B).”
- Also stated in: § Discussion · plain
“Interestingly, discontinuation of dietary red meat reduced plasma TMAO within 4 weeks.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Lastly, in contrast to TMAO, the fractional renal excretion of choline, betaine, carnitine, and c-butyrobetaine were significantly less than 100%, indicating that after filtering through the kidneys, most of these metabolites are reabsorbed, but less so following chronic dietary red meat exposure (Figure 5B-E).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
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In the paper
“It was interesting to note that following the initial 2 weeks defined run-in (baseline) diet, if a subject had a higher TMAO level at baseline, their TMAO level tended to be higher following other diet arms (compared with those with low TMAO at baseline, Figure 2C).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“A similar significant increase in urine levels of TMAO were noted following chronic ingestion of the red meat containing diet (P < 0.0001; Figure 3).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“In contrast, chronic exposure to the different diets substantially affected 24 h production of the d3-carnitine-derived metabolites (Figure 7A-E).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
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In the paper
“Interestingly, very modest but statistically significant reductions were noted in plasma betaine and urine choline concentrations following chronic consumption of the red meat diet compared with the non-meat or white meat diets (Figures 2A and 3).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“the fractional renal excretion of TMAO and the carnitine family of nutrient precursors and metabolites (carnitine, c-butyrobetaine, and crotonobetaine) were all dynamically (and differentially) regulated by the preceding dietary exposure.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“after 1 month of the red meat diet, fractional renal excretion of TMAO was significantly reduced”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“carnitine and both of the other carnitine derived gut microbial metabolites, c-butyrobetaine and crotonobetaine, all showed marked (2-5 fold) elevation in fractional renal excretion following the red meat diet.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“switching from a diet rich in red meat to either a white meat or non-meat protein source (yet maintaining same calories, and proportion of protein in the diet) can substantially reduce TMAO levels within several weeks.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“Elevated plasma TMAO levels are observed in subjects at risk for incident cardiovascular disease (CVD) development and adverse CVD events including heart attack, stroke, and death.[1][2][3][4]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature source
- Not checked yetcites [2] Tang, 2013, Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk, N Engl J Med source
- Not checked yetcites [3] Koeth, 2013, Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis, Nat Med source
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In the paper
“In a recent untargeted metabolomics study examining nearly 500 analytes to identify those that most closely correlate with renal function, C-mannosyl tryptophan and pseudouridine were identified as excellent renal functional surrogates.24”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
What the sources say
- Not checked yetcites [24] Sekula, 2016, A metabolome-wide association study of kidney function and disease in the general population, J Am Soc Nephrol source
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In the paper
“When the impact of order of the diets was examined on plasma and urine levels, no statistically significant difference in the observed effects of diet on the monitored metabolites was observed.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
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In the paper
“Trimethylamine N-oxide is generated via a metaorganismal pathway that begins with gut microbiota-dependent formation of trimethylamine (TMA) from TMA containing nutrient precursors (Figure 1A).[1][2][3]16”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature source
- Not checked yetcites [2] Tang, 2013, Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk, N Engl J Med source
- Not checked yetcites [3] Koeth, 2013, Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis, Nat Med source
plaindirect- Asserted: passes — The authors put it forward as true.
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In the paper
“Interestingly, in small cross-sectional observational studies, plasma levels of TMAO were modestly increased in omnivores relative to vegans/vegetarians, and in recent clinical challenge studies, TMA and TMAO generation from oral carnitine was observed to be substantially reduced in vegans/vegetarians.3,19”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
plaincorrelational- Asserted: passes — The authors put it forward as true.
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In the paper
“Consequently, a diet enriched in meat, particularly red meat, has higher content of both choline and carnitine nutrient precursors for TMA and TMAO generation.1,3”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
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In the paper
“Thus, decreasing systemic levels of TMAO has become a rational potential therapeutic strategy for decreasing risks for the development and progression of atherosclerotic heart disease.8,[13][14][15]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [8] Wang, 2015, Non-lethal inhibition of gut microbial trimethylamine production for the treatment of atherosclerosis, Cell source
- Not checked yetcites [13] Roberts, 2018, Development of a gut microbe-targeted nonlethal therapeutic to inhibit thrombosis potential, Nat Med source
- Not checked yetcites [14] Brown, 2018, Microbial modulation of cardiovascular disease, Nat Rev Microbiol source
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In the paper
“One potential candidate for this is the metaorganismal TMAO pathway.1,14,15”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature source
- Not checked yetcites [14] Brown, 2018, Microbial modulation of cardiovascular disease, Nat Rev Microbiol source
- Not checked yetcites [15] Brown, 2017, Targeting of microbe-derived metabolites to improve human health: the next frontier for drug discovery, J Biol Chem source
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In the paper
“Such findings arguably suggest that factors alternative to traditional CVD risk factors exist to help explain the association observed between red meat ingestion and heightened CVD risks.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“These findings appear to be robust, as they were observed using multiple different indices of renal function beyond creatinine (C-mannosyl tryptophan, pseudouridine, and SDMA).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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In the paper
“which would contribute to the observed rise in plasma TMAO levels.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
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- Based: passes — The paper gives a reason why it holds.
In the paper
“In one meta-analysis involving >25 000 subjects cumulatively with a mean follow-up duration amongst all studies examined of 4.3 ± 1.5 years, the relative risk for all-cause mortality was calculated to increase by 7.6% per each 10 lmol/L increment of TMAO.[10][11][12]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [10][11][12]
plaindirectn = 25,000- Asserted: passes — The authors put it forward as true.
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None of the sources cited for this claim have been checked yet.
In the paper
“recent human observational and interventional studies show that TMAO levels can increase substantially (>10 lM) with chronic supplementation.4,5”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
- It may state two separate claims as one. 27
- Probably not a substantial claim. 10
The sources with a verdict support this claim; the rest weren’t checked yet, have no full text we could read, or their verdicts aren’t rated yet.
In the paper
“Notably, a clinical prognostic value of TMAO has been supported by multiple meta-analyses reaffirming that elevated circulating TMAO levels are associated with both CVD and mortality risks across multiple cohorts and continents.[10][11][12]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [10] Schiattarella, 2017, Gut microbe-generated metabolite trimethylamine-N-oxide as cardiovascular risk biomarker: a systematic review and dose-response meta-analysis, Eur Heart J source
- Supportedcites [11] Qi, 2018, Circulating trimethylamine N-oxide and the risk of cardiovascular diseases: a systematic review and meta-analysis of 11 prospective cohort studies, J Cell Mol Med source
The Discussion reports that a meta-analysis of 11 prospective cohorts found higher baseline TMAO associated with increased cardiovascular-event and all-cause mortality risks. The Results (Study characteristics) place those cohorts in North America, Europe and New Zealand. The paper describes this as potential prognostic power, while cautioning that further studies are needed to establish prognostic efficacy. (LLM, conf=0.88)
- Supportedcites [12] Heianza, 2017, Gut microbiota metabolites and risk of major adverse cardiovascular disease events and death: a systematic review and meta-analysis of prospective studies, J Am Heart Assoc source
The Discussion reports that high circulating TMAO was associated with increased risks of major adverse cardiovascular events and all-cause death in a meta-analysis of prospective studies. The Strengths and Limitations section says participants came mainly from Europe and the United States, supporting the claim’s cross-continent scope. The paper cautions that its results may not apply to other racial or ethnic groups. (LLM, conf=0.92)
boostedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
The cited sources support only part of this claim — read each source’s verdict below.
In the paper
“Some of these TMA containing compounds can participate in TMA/TMAO formation in a gut microbiota-dependent manner, and also be generated by gut microbiota metabolism of L-carnitine.1,3,16,19”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Partly supportedcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature sourceExperimental — accuracy not yet measured
The Results section on TMAO formation from dietary phosphatidylcholine reports an obligate role for gut microbiota and the pathway PC → choline → TMA → TMAO. The Discussion also describes gut-flora-dependent TMA formation from trimethylamine-containing species. Our copy does not support the additional claim that these compounds are generated by gut microbiota metabolism of L-carnitine (searched: L-carnitine, carnitine). No page numbers are provided in the indexed passages. (LLM, conf=0.88)
- Partly supportedcites [3] Koeth, 2013, Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis, Nat Med sourceExperimental — accuracy not yet measured
The Results section, “TMAO production from dietary L-carnitine is inducible” (page unavailable), shows that gut microbiota are required to produce TMA and TMAO from L-carnitine in mice. The cited passages do not establish that other TMA-containing compounds are both generated from L-carnitine and subsequently participate in TMA/TMAO formation. (LLM, conf=0.82)
- Supportedcites [16] Koeth, 2014, γ-butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO, Cell Metab source
The Results section identifies γ-butyrobetaine (γBB) as a gut-microbial product of L-carnitine and an intermediate subsequently converted to TMA and TMAO. The Discussion likewise describes the L-carnitine → γBB → TMA pathway, followed by host conversion of TMA to TMAO. (LLM, conf=0.92)
- Supportedcites [19] Koeth, 2018, L-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans, J Clin Invest source
The Discussion states that γ-butyrobetaine (γBB) is produced by gut microbiota-dependent metabolism of ingested l-carnitine in humans and is an intermediate in TMAO formation. It also describes the microbial conversion of γBB to TMA, supporting both parts of the attributed claim. (LLM, conf=0.94)
plaindirect- Asserted: passes — The authors put it forward as true.
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- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
- Partly supported
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“First, compared to the other metabolites, the fractional excretion of TMAO was found to be both higher, and to demonstrate a remarkably broader range of values extending from nearly zero to over 700%, with a sizable proportion of subjects (almost half) showing >100%, particularly following the white meat and non-meat diet interventions.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
boostedcorrelational- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Interestingly, examination of the carnitine content of the diets (Supplementary ma- terial online, Table S1) reveals the baseline diet had 2 Â the carnitine level (56 mg) of the non-meat (high-saturated fat) diet (22 mg).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Similarly, no changes in plasma concentrations of other TMA containing compounds (choline, carnitine, cbutyrobetaine, and crotonobetaine; all P > 0.05, Figure 4B and D-F) were noted with high-vs.low-saturated fat except for a modest reduction in betaine levels with increased saturated fat (P < 0.05; Figure 4C).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We also noted that following the red meat diet, subjects showed a modest but significant (P = 0.006; Supplementary material online, Table S3) increase in serum creatinine (still within the normal range), while urine creatinine concentrations were increased (within normal range).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Notably, in contrast to creatinine, none of the surrogate indicators of renal function showed significant changes in plasma or urine levels based on diet, and all were highly correlated with creatinine (Supplementary material online, Tables S3 and S4).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In analyses examining the relationship between plasma and urine levels of TMAO, plasma TMAO levels were highly correlated with concurrently collected spot urine TMAO concentration (r = 0.41, P < 0.0001; N = 113) or urine TMAO/creatinine (r = 0.55, P < 0.0001; N = 113), and 24 h urine TMAO collections (r = 0.74, P < 0.001; N = 13).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
plaincorrelationaln = 113 ·- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast, no significant change in renal clearance of choline and only modest changes with betaine were observed among the three diets (Figure 5C).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“On average, plasma TMAO levels increased approximately three-fold (P < 0.0001) during the red meat diet, compared with the white meat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .or non-meat diets, with some subjects showing over a 10-fold increase (Figure 2A).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Results
plaindirect- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“this in- crease was substantially less than the 3.8-fold and 7.9-fold higher car- nitine content present in the red meat diet compared with the white meat and non-meat diets, respectively (Supplementary material on- line, Table S1).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plain- Asserted: passes — The authors put it forward as true.
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It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“While the total choline content of the red meat diet provided approximately 15% and 28% more compared with the average daily total choline content of the white meat and non-meat diets, respectively (Supplementary material online, Table S1)”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“subjects experienced on average an absolute change in median TMAO level of 5.9 lM and 5.7 lM during the red meat diet arm (compared with non-meat and white meat diets, respectively)”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Trimethylamine N-oxide (TMAO) is a gut microbiota-generated metabolite with mechanistic links to the pathogenesis of atherosclerotic heart disease.[1][2][3][4][5]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature source
- Not checked yetcites [2] Tang, 2013, Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk, N Engl J Med source
- Not checked yetcites [3] Koeth, 2013, Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis, Nat Med source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Carnitine is enriched in red meat, 3 and higher total choline content is found in beef and other meats, liver, and egg yolks.17”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Beyond choline and carnitine, potential nutrient precursors for TMA production have been reported, including the carnitine related metabolites c-butyrobetaine and crotonobetaine, and the choline oxidation product betaine.1,16,19”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [1] Wang, 2011, Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease, Nature source
- Not checked yetcites [16] Koeth, 2014, γ-butyrobetaine is a proatherogenic intermediate in gut microbial metabolism of L-carnitine to TMAO, Cell Metab source
- Not checked yetcites [19] Koeth, 2018, L-Carnitine in omnivorous diets induces an atherogenic gut microbial pathway in humans, J Clin Invest source
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Based upon the many epidemiological and nutrition studies suggesting a positive association between red meat ingestion and CVD risks, [27][28][29][30][31][32][33] most dietary recommendations advise limiting red meat ingestion.26”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [26] Piepoli, 2016, 2016 European guidelines on cardiovascular disease prevention in clinical practice: the Sixth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of 10 societies and by invited experts). Developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR), Eur Heart J source
- Not checked yetcites [27] Abete, 2014, Association between total, processed, red and white meat consumption and all-cause, CVD and IHD mortality: a meta-analysis of cohort studies, Br J Nutr source
- Not checked yetcites [28] O'Connor, 2017, Total red meat intake of >/=0.5 servings/d does not negatively influence cardiovascular disease risk factors: a systemically searched meta-analysis of randomized controlled trials, Am J Clin Nutr source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Moreover, adherence to a red meat diet raises systemic TMAO levels by three different mechanisms: (i) enhanced nutrient density of dietary TMA precursors; (ii) increased microbial TMA/TMAO production from carnitine, but not choline; and (iii) reduced renal TMAO excretion.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“This dietary intervention study had a randomized three-period crossover design.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Trial participants and study designs
plain- Asserted: passes — The authors put it forward as true.
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- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Lastly, in contrast to TMAO, the fractional renal excretion of choline, betaine, carnitine, and c-butyrobetaine were significantly less than 100%, indicating that after filtering through the kidneys, most of these metabolites are reabsorbed, but less so following chronic dietary red meat exposure (Figure 5B-E).”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“Studies have also shown dose-dependent TMA/TMAO formation with egg ingestion.2,18”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Introduction
What the sources say
- Not checked yetcites [2] Tang, 2013, Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk, N Engl J Med source
- Not checked yetcites [18] Miller, 2014, Effect of egg ingestion on trimethylamine-N-oxide production in humans: a randomized, controlled, dose-response study, Am J Clin Nutr source
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“However, some recent meta-analyses suggest the association between red meat ingestion and adverse changes to traditional CVD risk factors is not as strong, 28 despite the relatively consistent association with hard endpoints like heart attack, stroke, mortality, and CVD development.[29][30][31][32][33]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [28] O'Connor, 2017, Total red meat intake of >/=0.5 servings/d does not negatively influence cardiovascular disease risk factors: a systemically searched meta-analysis of randomized controlled trials, Am J Clin Nutr source
- Not checked yetcites [29] Schwingshackl, 2017, Food groups and risk of all-cause mortality: a systematic review and meta-analysis of prospective studies, Am J Clin Nutr source
- Not checked yetcites [30] Haring, 2017, Red meat consumption and cardiovascular target organ damage (from the Strong Heart Study), J Hypertens source
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“beyond quantity, the quality of diet composition (with respect to protein source, but not saturated fat content) impacts overall TMAO metabolism and excretion.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“Reduced urine TMAO levels were recently reported in an observational study among subjects following a Mediterranean diet in a post hoc cross-sectional analysis comparing omnivores vs. vegetarians or vegans 35 ; moreover, a trend towards reduced urinary TMAO levels was observed among subjects with increased reported compliance with the Mediterranean diet (based on the PREDIMED trial compliance tool”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [35] De Filippis, 2016, High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome, Gut source
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Fractional excretion calculations utilized creatinine plasma and urine concentrations, which varied based on diet, though we also quantified three separate alternative metabolites identified to serve as surrogate markers of renal function, and observed qualitatively comparable results.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Limitations
plaincorrelational- Asserted: passes — The authors put it forward as true.
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- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“the increases in plasma TMAO observed with the red meat diet would correspond to an approximate 4.5% increase in relative risk of mortality compared with the non-meat diet, and a 4.3% difference in mortality compared with white meat diet.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
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It may state two separate claims as one.
- The authors state this as an assumption: The changes in TMAO observed after one month of diet can be extrapolated to the mean follow-up of 4.3 years used in the meta-analysis.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“the present studies are the first to directly explore the relationship of dietary protein source to plasma TMAO levels with defined isocaloric randomized diets, and the time needed to reduce TMAO levels with dietary changes.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The present studies thus suggest that a diet rich in red meat would be associated with heightened TMAO levels, and potential heightened thrombotic event risk.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
hedgedcorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“numerous epidemiological studies show a dose-dependent heightened risk of thrombotic events, CVD, and mortality risks with red meat consumption.[29][30][31][32][33]”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [29][30][31][32][33]
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“The kidney is an important organ to maintain homoeostasis of plasma metabolites, 23 yet little is known about factors impacting renal excretion of TMAO or its related metabolites.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Chronic dietary exposure to red meat diet differentially impacts fractional renal excretion of trimethylamine N-oxide vs. carnitine and its metabolites
What the sources say
- Not checked yetcites [23] Thurau, 1964, Autoregulation of renal blood flow and glomerular filtration rate, including data on tubular and peritubular capillary pressures and vessel wall tension, Circ Res
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Only two visits of blood and urine for each diet arm were collected, which may not reflect the total intra-individual variability in subjects.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Limitations
hedged- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“The Mediterranean diet in the PREDIMED trial, which showed a 30% reduction in CVD risk, was characterized by avoidance of red meat as a protein source.36,37”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
- Not checked yetcites [36] Estruch, 2013, Primary prevention of cardiovascular disease with a Mediterranean diet, N Engl J Med source
- Not checked yetcites [37] Estruch, 2018, Primary prevention of cardiovascular disease with a Mediterranean diet supplemented with extra-virgin olive oil or nuts, N Engl J Med source
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: unclear — It is unclear whether the paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“TMAO has been shown to directly interact with platelets (human and murine), increasing their responsiveness, and promoting a prothrombotic phenotype.4,5”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Discussion
What the sources say
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Blood collection time after meal was not controlled, which may lead to fluctuation of plasma metabolite levels.”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Limitations
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
The paper relies on this without support.
Few studies have systematically explored the influence of chronic dietary patterns on TMA and TMAO production, metabolism, and renal excretion.
“Few studies have systematically explored the influence of chronic dietary patterns on TMA and TMAO production, metabolism, and renal excretion.”
The paper relies on this without support.
The direct contribution of TMAO to CVD pathogenesis in humans is unclear.
“the direct contribution of TMAO to CVD pathogenesis in humans is unclear, and the impact of dietary interventions on TMAO have not been extensively investigated.”
The paper relies on this without support.
The impact of dietary interventions on TMAO has not been extensively investigated.
“the direct contribution of TMAO to CVD pathogenesis in humans is unclear, and the impact of dietary interventions on TMAO have not been extensively investigated.”
The paper relies on this without support.
Little is known about factors impacting renal excretion of TMAO or its related metabolites.
“yet little is known about factors impacting renal excretion of TMAO or its related metabolites.”
The authors state this as an assumption.
The changes in TMAO observed after one month of diet can be extrapolated to the mean follow-up of 4.3 years used in the meta-analysis.
“assuming changes observed following 1 month of diet can be extended to the mean length of follow-up (4.3 year) in the meta-analysis”
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“There are, however, safety concerns about augmenting dietary protein above the 0.8 g·kg−1·d−1 range, especially from animal sources, because of concerns of accelerating coronary artery disease and HF incidence, as well as the potential for accelerating CKD progression.123–125”
From Malnutrition and Cachexia in Inpatients With Acute Cardiac Conditions: A Scientific Statement From the American Heart Association (2026) · cites this paper as [124]
Experimental — accuracy not yet measuredIn the citing paper
“A randomized controlled trial found that chronic ingestion of red meat, but not white meat or non-meat, increased plasma and urine levels of TMAO.142”
From Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer (2020) · cites this paper as [142]
In the citing paper
“In a recent human dietary intervention study examining protein source (red meat vs white meat vs non-meat), substantially higher levels of circulating TMAO were observed when subjects consumed a red meat diet (equivalent to 8oz of steak daily for 1 month)111.”
From Gut microbiota and cardiovascular disease. (2020) · cites this paper as [111]
In the citing paper
“In addition to having enhanced nutrient density of TMA(O) precursors (including carnitine), isotope tracer studies showed the red meat rich diet induced functional remodeling of the gut microbial community to enhance carnitine→→TMA transformation, but not choline→TMA generation111.”
From Gut microbiota and cardiovascular disease. (2020) · cites this paper as [111]
In the citing paper
“The TMAO pathway is an excellent example of this, given the nutrient precursors are more abundant in a Western diet, and diets rich in phosphatidylcholine and carnitine are associated with heightened levels of TMAO, whereas vegetarian or vegan diets have reduced nutrient precursors111, 118.”
From Gut microbiota and cardiovascular disease. (2020) · cites this paper as [111]
In the citing paper
“Notably, however, TMAO levels appear to be driven more so by the gut microbial community composition than by the dietary intervention, and significant variation in TMAO production among individuals on a given diet is observed14, 111.”
From Gut microbiota and cardiovascular disease. (2020) · cites this paper as [111]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Trial participants and study designs
“each separated by a 2-7 weeks washout period”
§ Impact of chronic dietary red meat, white meat, or non-meat protein on trimethylamine N-oxide metabolism and renal excretion in healthy men and women > Limitations
“with 2-week wash-out diets between each intervention dietary period”
Citations
Cites
2 retracted
RETRACTED: Primary Prevention of Cardiovascular Disease with a Mediterranean Diet
Estruch, R., Ros, E., Salas-Salvadó, J., Covas, M.-I., Corella, D., Arós, F., Gómez-Gracia, E., Ruiz-Gutiérrez, V., Fiol, M., Lapetra, J., et al. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1200303 · Cited by 4,257
RetractedEstruch, R., Ros, E., Salas-Salvadó, J., Covas, M.-I., Corella, D., Arós, F., Gómez-Gracia, E., Ruiz-Gutiérrez, V., Fiol, M., Lapetra, J., et al. (2018) · New England Journal of Medicine · doi:10.1056/nejmc1806491 · Cited by 1,008
RetractedEuropean Guidelines on cardiovascular disease prevention in clinical practice (version 2012)
Authors/Task Force Members:, Perk, J., De Backer, G., Gohlke, H., Graham, I., Reiner, Ž., Verschuren, M., Albus, C., Benlian, P., Boysen, G., et al. (2012) · European Heart Journal · doi:10.1093/eurheartj/ehs092 · Cited by 8,490
2016 European Guidelines on cardiovascular disease prevention in clinical practice
Piepoli, M. F., Hoes, A. W., Agewall, S., Albus, C., Brotons, C., Catapano, A. L., Cooney, M.-T., Corrà, U., Cosyns, B., Deaton, C., et al. (2016) · European Heart Journal · doi:10.1093/eurheartj/ehw106 · Cited by 6,457
Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease
Wang, Z., Klipfell, E., Bennett, B. J., Koeth, R., Levison, B. S., DuGar, B., Feldstein, A. E., Britt, E. B., Fu, X., Chung, Y.-M., et al. (2011) · Nature · doi:10.1038/nature09922 · Cited by 5,597
Self-citationIntestinal microbiota metabolism of l-carnitine, a nutrient in red meat, promotes atherosclerosis
Koeth, R. A., Wang, Z., Levison, B. S., Buffa, J. A., Org, E., Sheehy, B. T., Britt, E. B., Fu, X., Wu, Y., Li, L., et al. (2013) · Nature Medicine · doi:10.1038/nm.3145 · Cited by 4,386
Self-citationEstruch, R., Ros, E., Salas-Salvadó, J., Covas, M.-I., Corella, D., Arós, F., Gómez-Gracia, E., Ruiz-Gutiérrez, V., Fiol, M., Lapetra, J., et al. (2018) · New England Journal of Medicine · doi:10.1056/nejmoa1800389 · Cited by 3,616
Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk
Tang, W. H. W., Wang, Z., Levison, B. S., Koeth, R. A., Britt, E. B., Fu, X., Wu, Y., & Hazen, S. L. (2013) · New England Journal of Medicine · doi:10.1056/nejmoa1109400 · Cited by 3,400 · cited 1×
“Studies have also shown dose-dependent TMA/TMAO formation with egg ingestion.(2,18) Beyond choline and carnitine, potential nutrient precursors for TMA production have been reported, including the carnitine related metabolites c-butyrobetaine and crotonobetaine, and the choline oxidation product betaine.”
BackgroundSelf-citationGut Microbial Metabolite TMAO Enhances Platelet Hyperreactivity and Thrombosis Risk
Zhu, W., Gregory, J. C., Org, E., Buffa, J. A., Gupta, N., Wang, Z., Li, L., Fu, X., Wu, Y., Mehrabian, M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.02.011 · Cited by 1,968
Self-citationDe Filippis, F., Pellegrini, N., Vannini, L., Jeffery, I. B., La Storia, A., Laghi, L., Serrazanetti, D. I., Di Cagno, R., Ferrocino, I., Lazzi, C., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309957 · Cited by 1,638
Cited by
Sorted by citations
Gut microbiota and cardiovascular disease.
Witkowski, M., Weeks, T. L., & Hazen, S. L. (2020) · Circulation Research · doi:10.1161/circresaha.120.316242 · Cited by 1,051
Self-citationTargeting inflammation in atherosclerosis — from experimental insights to the clinic
Soehnlein, O., & Libby, P. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00198-1 · Cited by 1,085
Targher, G., Byrne, C. D., & Tilg, H. (2020) · Gut · doi:10.1136/gutjnl-2020-320622 · Cited by 879
“89”
Influence of the Gut Microbiome, Diet, and Environment on Risk of Colorectal Cancer
Song, M., Chan, A. T., & Sun, J. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.06.048 · Cited by 752
Functions of Gut Microbiota Metabolites, Current Status and Future Perspectives
Liu, J., Tan, Y., Cheng, H., Zhang, D., Feng, W., & Peng, C. (2022) · Aging and disease · doi:10.14336/ad.2022.0104 · Cited by 529
“disease, obesity, atherosclerosis, diabetes, heart failure, hypertension [37-39]”
Background
Metadata
- Authors
- Wang, Z., Bergeron, N., Levison, B. S., Li, X. S., Chiu, S., Jia, X., Koeth, R. A., Li, L., Wu, Y., Tang, W. H. W., Krauss, R. M., & Hazen, S. L.
- Affiliations
- Cleveland Clinic (US)
- Touro University California (US)
- Department of Atherosclerosis Research, Children’s Hospital Oakland Research Institute, Martin Luther King Jr Way, Oakland, CA, USA
- Cleveland State University (US)
- Corresponding author
- Hazen, Stanley L
- ORCID
- Venue
- European Heart Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-12-10
- Volume
- 40
- Issue
- 7
- Pages
- 583-594
- ISSN
- 0195-668X (ISSN-L)
- 1522-9645
- PMC
- PMC6374688
- OpenAlex
- W2904124435
- Semantic Scholar
- e6c31002dc7272f769757169c410825c0b0308a3
- Cited by
- 496
- References
- 40
- Citations by year
- 2026: 62 · 2025: 70 · 2024: 62 · 2023: 59 · 2022: 72 · 2021: 73 · 2020: 68 · 2019: 28 · 2018: 1
- FWCI
- 15.11
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Heart Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Touro Scholar (Touro College) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (HL103866, R01 HL126827, R01 DK106000, RO1 HL106003, R01 HL130819)
- Leducq Foundation
- Clinical and Translational Science Unit
- 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 › Agricultural and Biological Sciences › Animal Science and Zoology › Meat and Animal Product Quality
- Keywords
- trimethylamine N-oxide, red meat, white meat, L-carnitine, choline, gut microbiota, renal excretion, saturated fat, dietary protein, isotope tracers
- MeSH terms
- Red Meat, Adult, Aged, Animals, Diet, Dietary Proteins, Feeding Behavior, Female, Humans, Male, Methylamines, Middle Aged, Poultry, Reference Values, Cross-Over Studies, Young Adult, Renal Elimination
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.
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Statistics and arithmetic are recomputed, not judged.
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