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Host microbiota constantly control maturation and function of microglia in the CNS
Open accessAbstract
As the tissue macrophages of the CNS, microglia are critically involved in diseases of the CNS. However, it remains unknown what controls their maturation and activation under homeostatic conditions. We observed substantial contributions of the host microbiota to microglia homeostasis, as germ-free (GF) mice displayed global defects in microglia with altered cell proportions and an immature phenotype, leading to impaired innate immune responses. Temporal eradication of host microbiota severely changed microglia properties. Limited microbiota complexity also resulted in defective microglia. In contrast, recolonization with a complex microbiota partially restored microglia features. We determined that short-chain fatty acids (SCFA), microbiota-derived bacterial fermentation products, regulated microglia homeostasis. Accordingly, mice deficient for the SCFA receptor FFAR2 mirrored microglia defects found under GF conditions. These findings suggest that host bacteria vitally regulate microglia maturation and function, whereas microglia impairment can be rectified to some extent by complex microbiota.
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“perturbations of the gut microbiota by antibiotics systemically produce altered immune responses in experimental models, notably toward a pro-inflammatory profile (6).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Recent studies have shown that GF mice display deficits in microglia maturation and function, while recolonization or administration of key gut microbiota metabolites such as SCFAs restore microglial function”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“As stated earlier, SCFAs have been shown to ameliorate deficits in microglia morphology and immaturity as seen in GF mice (Erny et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In contrast, the absence of a complex host microbiota (when using GF animals or antibiotic-treated mice) increased microglial populations, caused defects in microglia maturation, activation state and differentiation, altered microglia morphology (with longer processes and increased branching, terminal points and clubbing at synaptic boutons), and compromised immune response to bacterial or viral”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Erny et al. 147 illustrated that germ-free animals display global deficiency in microglia and the genes needed to express type I interferon receptors such as Janus kinase 3 (Jak3) and signal transducer and activator of transcription 1 (Stat1), were reduced.147”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [147]
Experimental — accuracy not yet measured
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
“The function of microglia can be restored by the reconstruction of gut microbiota or their metabolites, indicating that microbiota may also be involved in the activity of the innate immune system in the brain via microbial metabolites and intestinal secretions.147”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [147]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In addition, SCFAs from intestinal microbiota are key molecules regulating the maturation, morphology and function of microglia.147”
From The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options (2021) · cites this paper as [147]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Microorganisms influence the brain through their ability to produce and modify metabolic, immunological and neurochemical factors in the gut that ultimately impact on the central nervous system59.”
From Association between attention-deficit/hyperactivity disorders and intestinal disorders: A systematic review and Meta-analysis (2025) · cites this paper as [59]
The cited source says what the claim attributes to it.
In the citing paper
“Microorganisms can influence CNS processes bidirectionally via the vagus nerve (12) and through modulation of the immune system (6), the hypothalamic-pituitary-adrenal (HPA) axis (13, 14), and tryptophan metabolism (15), along with their ability to synthetize a number of neurotransmitters (16–18) and produce metabolites, such as short-chain fatty acids (SCFAs), that possess neuroactive properties”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
The cited source says what the claim attributes to it.
In the citing paper
“it plays a major role in the bidirectional communication between the GI tract and the central nervous system (CNS).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
The cited source says what the claim attributes to it.
In the citing paper
“While microglia from specific pathogen-free (SPF) mice shows normal maturation and function, non-colonized young GF mice exhibit stunted microglia under homeostatic conditions.”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
The cited source says what the claim attributes to it.
In the citing paper
“the gut microbiota seems to play a pivotal role in the development and functionality of the immune system in the CNS.”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
The cited source says what the claim attributes to it.
In the citing paper
“Recently, it was determined that a diverse GI microbiota is necessary for the maintenance of, and maturation of, microglia in a healthy functional state (Erny et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
The cited source says what the claim attributes to it.
In the citing paper
“This is supported by observations in mice, where host microbiota control the maturation and function of microglia 33 .”
From Transcriptomic analysis of purified human cortical microglia reveals age-associated changes (2017) · cites this paper as [33]
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“the oral application of a mixture of the three major SCFAs acetate, propionate, and butyrate was sufficient to drive maturation of microglia in GF mice (6).”
From The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication (2020) · cites this paper as [6]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“In addition, FFAR2 transgenic mice have severely malformed microglia even though microglia do not express FFAR2, indicating that FFAR2 plays an indirect role in microglia function and homeostasis (Erny et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
Experimental — accuracy not yet measuredIn the citing paper
“However, the microglial defects and immaturity were partially restored by recolonization with complex microbiota and SCFAs supplementation.191”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [191]
In the citing paper
“Under homeostatic conditions, the gut microbiome is responsible for regulating microglial maturation and activation via short-chain fatty acids (SCFAs) release.190,191”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [191]
In the citing paper
“It was reported that the FFAR2-deficient SPF mice developed microglial defects resembling GF mice.191”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [191]
In the citing paper
“Thus, the microbiota is essential for microglia maturation and function.”
From Microglia Function in the Central Nervous System During Health and Neurodegeneration (2017) · cites this paper as [52]
In the citing paper
“Concurrently, genes highly expressed in microglia during early developmental stages that promote cell proliferation and survival, including Csf1r and Ddit4, are aberrantly up-regulated in microglia isolated from adult GF mice.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“The immature gene expression profile resulting from the absence of gut microbiota contributes to the inability of microglia to properly respond to immunostimulants such as LPS and the lymphocytic choriomeningitis virus, both of which failed to elicit an appropriate activation response in microglia from GF mice (Erny et al., 2015).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Consistent with patterns observed prenatally, microglia from adult GF mice, lacking constant postnatal input from gut microbiota, show distinct differences in density and morphology compared with those derived from SPF mice (Erny et al., 2015).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Microglial development appears arrested in GF mice, as supported by high expression of genes characteristic of early and premicroglia in microglia from adult GF mice.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Microglia from adult GF mice also display differential expression of genes associated with microglial maturation, including down-regulation of genes that regulate cell activation and immune system defense pathways, such as Mapk8, IL-1α, Ly86, Jak3, and Stat1, all of which are normally highly expressed in adult microglia (Fig. 1; Erny et al., 2015; Matcovitch-Natan et al., 2016).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“In SPF mice, a diverse gut microbiota promotes microglial development and maturation.”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Supplementation of drinking water with a mixture of three primary SCFAs (acetic acid, propionic acid, and butyric acid) rescued the immature genetic and morphological phenotype of microglia from GF mice (Erny et al., 2015).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“SPF mice lacking the free fatty acid receptor 2 (FFAR2), a GPCR required for SCFA signaling in the gut, exhibited a microglial phenotype similar to that observed in GF mice (Erny et al., 2015).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Given the requirement for constant input from the gut microbiota for normal microglial development and function, it is plausible that microbial effects on neural development and behavior may occur through changes in microglial activity (Erny et al., 2015; Thion et al., 2018).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Eradication of gut microbiota also alters microglial numbers, size, transcriptomes, and surveillance functions and downregulates host-defense genes147.”
From Microglia in neurodegeneration (2018) · cites this paper as [147]
In the citing paper
“Intestinal bacterial colonization regulates immune system maturation and development in the CNS.”
From Microglia in neurodegeneration (2018) · cites this paper as [147]
In the citing paper
“Recolonization with a complex microbiota or with microbiota-derived products partially restores microglial properties147.”
From Microglia in neurodegeneration (2018) · cites this paper as [147]
In the citing paper
“Studies using germ-free mice, antibiotic treatment, and selective microbial colonization suggest that the intestinal microbiota can regulate microglial maturation and function in the enteric and central nervous systems [37, 54].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [37]
In the citing paper
“Germ-free mice develop microglia with an immature phenotype, blunted response to inflammatory stimuli and defective immune response to infection (Erny et al., 2015).”
From Alzheimer Disease: An Update on Pathobiology and Treatment Strategies (2019) · cites this paper as Erny et al., 2015
In the citing paper
“Germ-free mice exhibited microglia dysfunction that could be rescued by treatment with SCFAs.”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Erny et al., 2015
In the citing paper
“Ffar2−/− mice had a similar defect, although no FFAR2 expression could be detected on microglia, leaving the connection between SCFAs and microglia unresolved (Erny et al., 2015).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Erny et al., 2015
In the citing paper
“Beyond intestinal macrophages, SCFAs have also been reported to be functionally important for microglia, a macrophage-like cell type of the central nervous system.”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Erny et al., 2015
In the citing paper
“although no FFAR2 expression could be detected on microglia”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Erny et al., 2015
In the citing paper
“A gut-brain axis exists involving both neural and metabolic communication that could affect microglia199.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [199]
In the citing paper
“Finally, the microbiome plays a central role in health and disease, and the host microbiome controls maturation and function of microglia199.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [199]
In the citing paper
“Animals raised in a germ-free environment or mice treated with broad-spectrum antibiotics develop dysfunctional microglia, an effect that can be ameliorated with short-chain fatty acids.”
From Microglial signatures and their role in health and disease (2018) · cites this paper as [199]
In the citing paper
“Erny and colleagues [257] demonstrated that proper functioning of the brain microglia needs the gut microbiome.”
From The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders (2021) · cites this paper as [257]
In the citing paper
“Interestingly, Erny and colleagues demonstrate that the microbiome is required for proper development and function of adult brain microglia (71).”
From Emerging Roles for the Gut Microbiome in Autism Spectrum Disorder (2017) · cites this paper as [71]
In the citing paper
“The microbiota contributes to microglia homeostasis, potentially mediated by signaling through SCFAs.240”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [240]
In the citing paper
“GF mice display marked defects in microglia structure and function and hence feature impaired CNS innate immune responses.240,241”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [240]
In the citing paper
“The transcriptomic profile can be shaped by intrinsic factors, such as age and sex, pathogenic and tissue-specific cues including protein aggregates, stress signals, nutrients, and external cues such as signals from the microbiota colonizing gastrointestinal and urogenital tracts [15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“Microglial transcriptomes are tightly regulated by multiple key transcription factors such as Sall1, Spi1, Mafb, and Mef2c [5, 15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“Accumulating evidence indicates that PU.1 expression significantly alters the microglia phenotypes via reshaping the gut microbiota landscape.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“RNA-seq analysis of microglia from GF mice revealed that microglia transcription factor PU.1 and survival factor CSF1R were significantly upregulated in microglia from GF mice [1, 15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“The immature phenotype of GF microglia could be corrected by microbiota recolonization [15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“gut symbiosis promoted the maintenance of microglia under homeostasis conditions, while germ-free (GF) condition led to impaired microglia maturation, differentiation and function [15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“while germ-free (GF) condition led to impaired microglia maturation, differentiation and function [15].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“The gut microbiome has emerged as a key regulator of the immune system and microglial physiology.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“Microglia are dysregulated in mice with dysbiosis, either due to microbial imbalance or maladaptation [15]”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [15]
In the citing paper
“iMGLs not cultured with neurons differentially expressed early microglia genes including FFAR2”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Erny et al., 2015
In the citing paper
“Microbes influence CNS processes via modulation of the nervous system (52), endocrine system (51, 126), and immune system (120), together with their ability to synthesize neurotransmitters (127–129) and produce metabolites (127, 130–132) ( Figure 1 ).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“The GM appears to influence microglial development and maturation (120, 121), and animal models have demonstrated downstream effects on various aspects of neurocognitive function (19, 45, 60, 114, 115).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“SCFAs can modify neuroinflammation by affecting the morphology and function of glial cells (120, 286, 289, 290).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“Antibiotic-treated and germ-free mice have pro-inflammatory systemic and CNS immune system responses (120, 267).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“SCFAs may also improve neuronal homeostasis and function by influencing neurotrophic factors such as nerve growth factor, glial cell line-derived neurotrophic factor, and BDNF (119–122).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“By administering SCFAs to germ-free mice, Erny et al. were able to rescue deficits in microglial immaturity and morphology (120).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [120]
In the citing paper
“Interestingly, impairments in microglia function were reversed by administration of SCFAs [38].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [38]
In the citing paper
“In a rodent study, germ-free mice had a decreased number of mature microglia in various brain areas when compared to mice with a normal microbiome [38].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [38]
In the citing paper
“In the central nervous system, SCFAs have additional roles, such as regulating maturity and function of microglia (macrophages in the brain that are part of the brain’s immune response) [56].”
From Effect of fecal microbiota transplant on symptoms of psychiatric disorders: a systematic review (2020) · cites this paper as [56]
In the citing paper
“Innate immunity is also regulated by the gut microbiota as evidenced by reduced numbers and compromised functions of antigen-presenting cells and microglia in germ-free animals60,69.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [60]
In the citing paper
“A lack of gut microbiota leads to deficient development of the GALT58 and abnormal systemic59 and central immunity60.”
From The gut microbiota and the brain–gut–kidney axis in hypertension and chronic kidney disease (2018) · cites this paper as [60]
In the citing paper
“A study demonstrated that treatment with microbial-produced short-chain fatty acids (SCFAs) could rescue microglial function impaired in GF animals [167].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [167]
In the citing paper
“Indeed, the mediation of certain behavioral phenotypes as a consequence of prolonged HPA axis activation involves the trafficking of monocyte from the spleen (Wohleb et al., 2014), a tissue with a high density of free fatty acid receptor type 2 (FFAR2) (Erny et al., 2015).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
In the citing paper
“These alterations in microglial phenotype were reversed with recolonization of gut microbiota, following six weeks co-habitation of GF mice with control mice.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Erny et al., 2015
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Metadata
- Authors
- Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermöhlen, O., Chun, E., Garrett, W. S., McCoy, K. D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I., & Prinz, M.
- Affiliations
- University of Freiburg (DE)
- Weizmann Institute of Science (IL)
- University of Cologne (DE)
- Technical University of Munich (DE)
- Johannes Gutenberg University Mainz (DE)
- Harvard University (US)
- University of Bern (CH)
- German Center for Infection Research (DE)
- Corresponding author
- Prinz, Marco
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2015-06-01
- Volume
- 18
- Issue
- 7
- Pages
- 965-977
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5528863
- OpenAlex
- W1515023627
- Cited by
- 3,569
- References
- 61
- Citations by year
- 2026: 403 · 2025: 393 · 2024: 413 · 2023: 380 · 2022: 472 · 2021: 407 · 2020: 345 · 2019: 250 · 2018: 195 · 2017: 156 · 2016: 118 · 2015: 32
- FWCI
- 89.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- PubMed Central (acceptedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion)
- OPUS (Augsburg University) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Deutsche Forschungsgemeinschaft (SFB 992, FOR1336)
- Bundesministerium für Bildung und Forschung
- National Cancer Institute (R01CA154426)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- host microbiota, microglia, microglial maturation, microglial homeostasis, germ-free mice, short-chain fatty acids, FFAR2, innate immune response, gut-brain axis, bacterial fermentation products, central nervous system
- MeSH terms
- Animals, Central Nervous System, Fatty Acids, Volatile, Female, Homeostasis, Immunity, Innate, Male, Mice, Inbred C57BL, Microglia, Receptors, G-Protein-Coupled, Mice, Microbiota
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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