The Role of Gut and Oral Microbiota in the Formation and Rupture of Intracranial Aneurysms: A Literature Review
Abstract
:1. Introduction
2. Exploring Pathways: Inflammation and Cerebral Aneurysm Formation, Gut–Brain Interactions, and Microbiome Analysis
2.1. The Role of Inflammation in Cerebral Aneurysm Formation
2.2. Potential Mechanisms of Gut–Brain Interaction
2.3. Methods of Analyzing the Microbiome
3. The Gut Microbiome and Intracranial Aneurysm Formation and Rupture
Study | Type | Medium | Intervention | Aim | Method | Result |
---|---|---|---|---|---|---|
Shikata et al., 2019 [52] | interventional study | mice | gut depletion by antibiotics in mice with IA induction vs. mice with normal gut and IA induction | - number and rupture rate of IAs; - number of macrophages in IA tissue; - mRNA levels of cytokines in IA tissue. | - immunohistochemistry; - RT-PCR. | - gut depletion reduced the incidence of IA (83% vs. 6%, p < 0.001) and rupture; - macrophage infiltration and mRNA levels of inflammatory cytokines were reduced with gut depletion. |
Li et al., 2020 [65] | case–control study | - humans - mice | - analysis of fecal samples of 140 UIA and 140 control patients; - 20 mice treated with UIA patient feces and 20 treated with control feces. | - comparison of gut microbiome of patients with UIAs and without; - test, if changes in the gut microbiota influence the progression of UIAs in vivo. | - metagenomic shotgun sequencing; - serum metabolomic analysis. | - Bacteroides ssp., Odoribacter splanchnicus, Clostridium ssp. were significantly enriched in the UIAs; - Hungatella hathewayi was enriched in the control group; - microbiome of UIAs was significantly dominated by unsaturated fatty acid biosynthesis; - microbiome of controls was dominated by amino acid synthesis; - treatment with feces from UIA patients increased the overall incidence of IAs (85% vs. 45%; p = 0.019) and rupture rate (82% vs. 22%; p = 0.009); - serum concentrations of 2 of 8 fatty acids and 8 of 38 amino acids differed in mice transplanted with feces from UIA patients and controls. |
Kawabata et al., 2022. [66] | multicenter, prospective case–control | humans | analysis of fecal samples of 28 RAs vs. 33 UIAs | comparison of gut microbiome of patients with UIAs and RAs | 16S rRNA sequencing | - gut microbiome profile of UIAs and RAs were significantly different; - Campylobacter ssp. and Campylobacter ureolyticus were significantly higher in the RA group. |
He et al., 2023. [67] | two-sample Mendelian randomization study | humans | database analysis of gut microbiome of patients with IA, UIA, SAH | association between the gut microbiome and the risk of IA, UIA, and SAH | inverse variance weighting approach | - Candidatus Soleaferrea decreased the risk of IA; - Holdemania and Olsenella increased risk of IA; - Lentisphaeria, Porphyromonadaceae, Bilophila, Fusicatenibacter, Ruminococcus sp. 1, Victivallales decreased risk of SAH; - Streptococcaceae increased risk of SAH; - Porphyromonadaceae, Bilophila decreased the risk of UIA; - Oxalobacteraceae, Adlercreutzia, Intestinimonas, Victivallis increased the risk of UIA. |
Ma et al., 2023. [68] | two-sample Mendelian randomization study | humans | database analysis of gut microbiome of UIA patients | association between the gut microbiome and the risk of UIA | inverse variance weighting approach | - Clostridia, Rhodospirillaceae, Adlercreutzia, Sutterella, Victivallis, Streptococcus, Peptostreptococcaceae increased risk of UIA; - Oscillospira, Paraprevotella decreased the risk of UIA. |
4. The Oral Microbiome and Intracranial Aneurysm Formation and Rupture
Study | Type | Medium | Intervention | Aim | Method | Result |
---|---|---|---|---|---|---|
Pyysalo et al., 2013. [71] | prospective cohort study | humans | analysis of RA tissue of 36 patients with SAH | assess the presence of oral and pharyngeal bacterial genome in RAs | qRT-PCR | - bacterial DNA was detected in 21/36 (58%); - DNA from endodontic bacteria was detected in 20/36 (56%) and from periodontal bacteria in 17/36 (47%); - DNA of the Streptococcus-mitis group was the most common. |
Pyysalo et al., 2016. [72] | prospective cohort study | humans | analysis of RA tissue of 42 patients and UIA tissue of 28 patients, tissue from healthy vessels and cardiac by-pass operations as controls | assess the presence of oral and pharyngeal bacterial DNA in RAs and UIAs | qRT-PCR | - bacterial DNA was detected in 49/70 (70%); - 29/42 (69%) of the RA tissue and 20/28 (71%) of the UIA tissue contained bacterial DNA of oral origin; - RA and UIA samples contained significantly more bacterial DNA than control samples. |
Pyysalo et al., 2018. [73] | prospective cohort study | humans | analysis of tissue from gingival pockets of 30 patients with RA and 60 with UIA | assess the presence of dental infectious foci and odontogenic bacteria in patients before surgical treatment of IA | qRT-PCR | - total of 43% had gingival pockets of 6 mm or deeper; - bacterial and Fusobacterium nucleatum DNA were significantly higher in the patients with ≥6 mm gingival pockets than patients without them. |
Inenaga et al., 2018. [74] | prospective cohort study | humans | analysis of saliva from 48 patients with CES, 151 with non-CES infarct, 54 with ICH, 43 with RA, and 97 with UIA vs. 79 healthy controls | assess the rate of Streptococcus mutans with collagen-binding protein, Cnm, in CES, non-CES infarct, ICH, RA, and UIA | PCR | - significantly high Cnm-positive rate was observed in CES, non-CES infarct, ICH and RA compared to controls. |
Aboukais et al., 2019. [75] | prospective cohort study | humans | analysis of IA tissue from 10 patients with RA and 20 with UIA, samples from STA, dura mater, and MCA as control | assess the presence of bacteria in the walls of UIAs and RAs | PCR | - no bacterial presence was found in the wall of aneurysms. |
Hallikainen et al., 2019. [76] | case series, case–control, prospective study | humans | oral examination of 42 patients with UIAs and 34 RAs compared to 5170 from prospective database | association of periodontitis with IA formation and SAH | multivariate logistic regression | - periodontitis, severe periodontitis, and gingival bleeding increased the risk of IAs significantly; severe periodontitis in ≥3 teeth or gingival bleeding increased the risk of SAH significantly. |
Hallikainen et al., 2021. [77] | prospective cohort study | humans | analysis of serum of 227 IA patients, compared to 1096 from prospective database | association of IgA and IgG against Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans with IA and SAH | ELISA | - high IgA against P. gingivalis and A. actinomycetemcomitans increased the risk of IA and SAH significantly; - high IgG levels against P. gingivalis and A. actinomycetemcomitans decreased the risk of IA and SAH significantly. |
Hallikainen et al., 2023. [78] | case–control, prospective study | humans | oral examination of 60 patients with UIA and 30 with RA compared to 5144 from prospective database | association of caries with IA formation and SAH | multivariate logistic regression | - caries does not increase the risk of IAs and SAH. |
5. Conclusions
6. Future Directions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Joerger, A.-K.; Albrecht, C.; Rothhammer, V.; Neuhaus, K.; Wagner, A.; Meyer, B.; Wostrack, M. The Role of Gut and Oral Microbiota in the Formation and Rupture of Intracranial Aneurysms: A Literature Review. Int. J. Mol. Sci. 2024, 25, 48. https://doi.org/10.3390/ijms25010048
Joerger A-K, Albrecht C, Rothhammer V, Neuhaus K, Wagner A, Meyer B, Wostrack M. The Role of Gut and Oral Microbiota in the Formation and Rupture of Intracranial Aneurysms: A Literature Review. International Journal of Molecular Sciences. 2024; 25(1):48. https://doi.org/10.3390/ijms25010048
Chicago/Turabian StyleJoerger, Ann-Kathrin, Carolin Albrecht, Veit Rothhammer, Klaus Neuhaus, Arthur Wagner, Bernhard Meyer, and Maria Wostrack. 2024. "The Role of Gut and Oral Microbiota in the Formation and Rupture of Intracranial Aneurysms: A Literature Review" International Journal of Molecular Sciences 25, no. 1: 48. https://doi.org/10.3390/ijms25010048