Symptomatic atherosclerosis is associated with an altered gut metagenome
Open accessAbstract
Recent findings have implicated the gut microbiota as a contributor of metabolic diseases through the modulation of host metabolism and inflammation. Atherosclerosis is associated with lipid accumulation and inflammation in the arterial wall, and bacteria have been suggested as a causative agent of this disease. Here we use shotgun sequencing of the gut metagenome to demonstrate that the genus Collinsella was enriched in patients with symptomatic atherosclerosis, defined as stenotic atherosclerotic plaques in the carotid artery leading to cerebrovascular events, whereas Roseburia and Eubacterium were enriched in healthy controls. Further characterization of the functional capacity of the metagenomes revealed that patient gut metagenomes were enriched in genes encoding peptidoglycan synthesis and depleted in phytoene dehydrogenase; patients also had reduced serum levels of β-carotene. Our findings suggest that the gut metagenome is associated with the inflammatory status of the host and patients with symptomatic atherosclerosis harbor characteristic changes in the gut metagenome. The gut microbiota has emerged as an environmental factor that can influence the development of obesity and diabetes. Here, Karlsson et al. report compositional and functional alterations of the gut metagenome in patients with symptomatic atherosclerosis.
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Short chain fatty acids are produced by microbiota from dietary fibers, affect host body energy homeostasis, and are protective against metabolic syndrome, type 2 diabetes mellitus, and atherosclerosis.
“Short chain fatty acids are produced by microbiota from dietary fibers, effect host body energy homeostasis, and are protective against metabolic syndrome, type 2 diabetes mellitus, and atherosclerosis.15,45–47”
From The Gut Microbiome Contributes to a Substantial Proportion of the Variation in Blood Lipids (2015) · cites this paper as [45]
Reanalysis of metagenomes from Karlsson and colleagues indicated increased abundances of bacteria exhibiting the potential to produce TMA by about a factor of 2 in symptomatic atherosclerosis patients (n = 12) compared to healthy controls (n = 13), with median values of 0.39 and 0.11% in patients versus 0.22 and 0% in controls for cutC and cntA, respectively.
“Our results indicated increased abundances of bacteria exhibiting the potential to produce TMA (by about a factor of 2) in the patient group where the abundances of key genes of both pathways were elevated (median values of 0.39 and 0.11% (patient group) versus 0.22 and 0% (controls) for cutC and cntA, respectively, as a percentage of bacteria calculated to exhibit the genes) (Additional file 8).”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [12]
Reanalysis of the dataset provided by Karlsson and colleagues indicated elevated abundances of potential TMA producers in atherosclerosis patients.
“Reanalysis of the dataset provided by Karlsson and colleagues [12] indicated elevated abundances of potential TMA producers in atherosclerosis patients”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [12]
Symptomatic atherosclerosis is associated with an altered gut microbiome.
“a metagenomic study suggested that symptomatic atherosclerosis was associated with an altered gut microbiome.8”
From Dysbiosis of gut microbiota with reduced trimethylamine-N-oxide level in patients with large-artery atherosclerotic stroke or transient ischemic attack (2015) · cites this paper as [8]
Individuals classified as enterotype 3, characterized by low levels of Bacteroides, have a higher incidence of symptomatic atherosclerosis.
“Individuals classified as enterotype 3, which is characterized by low levels of Bacteroides, 8 have a higher incidence of symptomatic atherosclerosis.1,9”
From <i>Bacteroides vulgatus</i> and <i>Bacteroides dorei</i> Reduce Gut Microbial Lipopolysaccharide Production and Inhibit Atherosclerosis (2018) · cites this paper as [9]
Diseases linked to dyslipidemia, such as non-alcoholic liver disease and atherosclerosis, are associated with changes in gut microbiota profile.
“Furthermore, diseases linked to dyslipidemia, such as non-alcoholic liver disease and atherosclerosis, are associated with changes in gut microbiota profile.”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [41]
Only a very small number of samples from patients with cardiovascular diseases have been analyzed.
“By contrast, only a very small number of samples from patients with cardiovascular diseases have been analyzed10.”
From The gut microbiome in atherosclerotic cardiovascular disease (2017) · cites this paper as [10]
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Intestinal Microbiota in Cardiovascular Health and Disease
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Self-citationRoseburia intestinalis: A Beneficial Gut Organism From the Discoveries in Genus and Species
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Statin therapy is associated with lower prevalence of gut microbiota dysbiosis
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“pylori cells [232]; Collinsella [233]; Roseburia and Eubacterium [233] Carnitine-butyrobetainetrimethylamine-N-oxide pathway [235]; cause vascular atherosclerosis by affecting lipid and hormonal homeostasis [82, 222]; formation of foam cell by inflammation [236, 237] L.”
InfluentialRole of the gut microbiota in type 2 diabetes and related diseases
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Gut Microbiota and Complications of Type-2 Diabetes
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Fecal Microbiota Transplantation in Neurological Disorders
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“, 2018), cerebral infarction (Karlsson et al., 2012; Yin et al., 2015), spinal cord injury (Gungor et al.”
Elevated circulating levels of succinate in human obesity are linked to specific gut microbiota
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“reporting decreased relative abundance of Roseburia and Eubacterium, known producers of butyrate [18].”
InfluentialThe gut microbiota modulates host amino acid and glutathione metabolism in mice
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Application of metagenomics in the human gut microbiome
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The effect of antibiotics on the composition of the intestinal microbiota—a systematic review
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The dormant blood microbiome in chronic, inflammatory diseases
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A Proinflammatory Gut Microbiota Increases Systemic Inflammation and Accelerates Atherosclerosis
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The Gut Microbiota and Unhealthy Aging: Disentangling Cause from Consequence
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Gut–organ axis: a microbial outreach and networking
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Mining the microbiota for microbial and metabolite-based immunotherapies
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The Role of the Immune System in Metabolic Health and Disease
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Fecal microbiota transplantation in metabolic syndrome: History, present and future
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“found in 2012 that atherosclerosis is associated with a different gut metagenome.(81) One mechanism of microbiota-mediated atherosclerosis induction that has been elucidated is through L-carnitine and phosphatidylcholine (from red meat, cheese and eggs).”
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Heart Failure is Associated with Depletion of Core Intestinal Microbiota
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“It is conceivable that depletion of these genera contributes to HF pathogenesis, as recent findings from other inflammatory diseases suggest: For example, Collinsella bacteria have been reported to be associated with systemic atherosclerosis and type 2 diabetes mellitus (T2DM).(34,35) Interestingly, this genus seems t…”
Specific gut microbiota features and metabolic markers in postmenopausal women with obesity
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The gut microbiota and metabolic disease: current understanding and future perspectives
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“In other gut microbiota-associated diseases and in silico predictions of the HIV microbiota, an increase in antioxidant pathways such as riboflavin, glutathione, and glutaminemetabolismhas been described and interpreted as the bacterial compensatory mechanism that attenuates the oxidative stress caused by epithelial d…”
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Composition Diversity and Abundance of Gut Microbiome in Prediabetes and Type 2 Diabetes
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Human gut microbiota community structures in urban and rural populations in Russia
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Microbiome and metabolome features of the cardiometabolic disease spectrum
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The gut microbiota: A treasure for human health
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“At the functional level, the gutmicrobiome of atherosclerosis patients were enriched in genes associated with peptidoglycan biosynthesis, whereas phytoene dehydrogenase genes were enriched in healthy subjects (Karlsson et al., 2012).”
Understanding the interactions between bacteria in the human gut through metabolic modeling
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Self-citationModulation of gut microbiota dysbioses in type 2 diabetic patients by macrobiotic Ma-Pi 2 diet
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Aging progression of human gut microbiota
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“Several studies have suggested that the gut microbiota can contribute to obesity and related metabolic diseases, such as type 2 diabetes, liver disease, and atherosclerosis (7,8,13,25-28).”
The Gut Microbiota (Microbiome) in Cardiovascular Disease and Its Therapeutic Regulation
Rahman, M. M., Islam, F., Harun-Or-Rashid, M., Mamun, A. A., Rahaman, M. S., Islam, M. M., Meem, A. F. K., Sutradhar, P. R., Mitra, S., Mimi, A. A., et al. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.903570 · Cited by 267 · see citing works
“Additionally, the toxic level of p-cresol sulfide has been demonstrated previously (Karlsson et al., 2012).”
InfluentialSmits, L. P., Kootte, R. S., Levin, E., Prodan, A., Fuentes, S., Zoetendal, E. G., Wang, Z., Levison, B. S., Cleophas, M. C. P., Kemper, E. M., et al. (2018) · Journal of the American Heart Association · doi:10.1161/jaha.117.008342 · Cited by 250 · see citing works
“The intestinal microbiota composition in patients with symptomatic CVD differs significantly from that in healthy controls.(1,2) Moreover, DNA from intestinal microbiota has been recovered from human atherosclerotic plaques, suggesting a potentially contributory role of gut microbiota to atherosclerosis.”
Nielsen, J. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061516-044757 · Cited by 252 · see citing works
“Gut bacteria are involved in the biosynthesis of different vitamins that are important for overall metabolism of the host, but they also produce bioactive molecules such as β-carotene that can protect against atherosclerosis (175).”
Self-citationBohn, T., Desmarchelier, C., Dragsted, L. O., Nielsen, C. S., Stahl, W., Rühl, R., Keijer, J., & Borel, P. (2017) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600685 · Cited by 252 · see citing works
“in diseased subjects [133], highlighting the potential role of the microbiota.”
Evolution, human-microbe interactions, and life history plasticity
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“(93) However the complex interactions between the gut microbiota and diet are only just beginning to be unravelled and it is clear that microbiota contribute to metabolic diseases such as obesity, diabetes and CVD,(94-97) as well as to inflammatory diseases and behavioral effects.”
Self-citationMicrobiota-mediated inflammation and antimicrobial defense in the intestine
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“Positive correlations between gut microbes belonging to the genus Collinsella and atherosclerosis (197) and negative correlations between Lactobacillales and the development of graft-versus-host disease following allogeneic hematopoietic stem cell transplantation have been found and suggest that the impact of microbio…”
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“Indeed, attempts to identify TMA-generating microbes by correlating either disease phenotypes or metabolite levels with changes in gut community composition have been unsuccessful (18, 57).”
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The role of intestinal microbiota in cardiovascular disease
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HIV and antiretroviral therapy-related fat alterations
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The Role of Gut Microbiota in Atherosclerosis and Hypertension
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- Authors
- Karlsson, F. H., Fåk, F., Nookaew, I., Tremaroli, V., Fagerberg, B., Petranovic, D., Bäckhed, F., & Nielsen, J.
- Affiliations
- Chalmers University of Technology (SE)
- University of Gothenburg (SE)
- Corresponding author
- Bäckhed, Fredrik
- Nielsen, Jens
- ORCID
- Venue
- Nature Communications
- Published
- 2012-12-04
- Volume
- 3
- Issue
- 1
- Pages
- 1245-1245
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC3538954
- OpenAlex
- W2163940893
- Semantic Scholar
- fa78fbe4819f11f57f8abcdc9460b2aceded402d
- Cited by
- 1,371
- References
- 48
- Citations by year
- 2026: 83 · 2025: 138 · 2024: 139 · 2023: 137 · 2022: 160 · 2021: 143 · 2020: 126 · 2019: 98 · 2018: 97 · 2017: 73 · 2016: 51 · 2015: 59 · 2014: 37 · 2013: 29
- FWCI
- 16.08
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (unspecified)
- Locations
- Nature Communications (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Chalmers Publication Library (Chalmers University of Technology) (submittedVersion)
- Chalmers Research (Chalmers University of Technology) (submittedVersion)
- Funders
- Stiftelsen för Strategisk Forskning
- Knut och Alice Wallenbergs Stiftelse
- Vetenskapsrådet
- Sahlgrenska Universitetssjukhuset
- Göteborgs Universitet
- Fondation Chalmers
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Keywords
- gut microbiota, gut metagenome, Collinsella, Roseburia, Eubacterium, carotid artery stenosis, cerebrovascular disease, peptidoglycan biosynthesis, phytoene desaturase, beta-carotene, inflammation, lipid accumulation
- MeSH terms
- Aged, Eubacterium, Female, Humans, Inflammation, Male, Oxidoreductases, Peptidoglycan, Case-Control Studies, beta Carotene, Actinobacteria, Gastrointestinal Tract, Atherosclerosis, Metagenome
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 ›
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