Chronic mesenteric ischemia-induced intestinal dysbiosis resolved after revascularization
Open accessAbstract
Objectives Chronic mesenteric ischemia (CMI) is a debilitating condition arising from intestinal malperfusion from mesenteric artery stenosis/occlusion. Mesenteric revascularization is the standard of care but carries substantial morbidity/mortality. The majority of perioperative morbidity is secondary to postoperative multiple organ dysfunction, potentially from ischemia/reperfusion injury. The intestinal microbiome is a dense community of microorganisms in the gastrointestinal tract that help regulate pathways ranging from nutritional metabolism to the immune response. We hypothesized that patients with CMI have microbiome perturbations that contribute to this inflammatory response and potentially normalize in the postoperative period. Methods A prospective study of CMI patients who underwent mesenteric bypass/stenting was conducted between 2019-2020. Stools were collected at 3 timepoints: pre-operative clinic, perioperatively within 14 days, and post-operative clinic >30 days post-revascularization. Stool samples from healthy controls were used for comparison. Microbiome was measured by 16S rRNA sequencing on an Illumina-MiSeq® sequence platform and analyzed using qiime2-dada2 bioinformatics pipeline with SILVA database. β-diversity was analyzed using principal coordinates analysis and permutational analysis of variance. α-diversity (microbial richness and evenness) was compared using non-parametric Mann-Whitney-U test. Microbial taxa unique for CMI patients versus controls were identified using the linear discriminatory analysis effect size (LEfSe) analysis. P <0.05 was considered statistically significant. Results Eight patients underwent mesenteric revascularization (25% male; average age: 71). Nine healthy controls were analyzed (78% male; average age: 55). Bacterial α-diversity (number of OTUs) was dramatically reduced in preoperative group versus controls (p=0.03); however, revascularization partially restored the species richness and evenness in perioperative and postoperative phases. Beta-diversity was only different between perioperative and post-operative groups (p=0.03). Further analyses revealed increased abundance of Bacteroidetes and Clostridia taxa pre-operatively and perioperatively compared to controls, which was reduced during post-operative period. Conclusion Patients with CMI have intestinal dysbiosis that resolves after revascularization. This is characterized by loss of alpha-diversity, which is restored perioperatively and is maintained postoperatively. This microbiome restoration demonstrates the importance of intestinal perfusion to sustain gut homeostasis and suggests that the microbiome modulation could be a possible intervention to ameliorate acute and sub-acute post-operative outcomes in these patients.
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Patients with chronic mesenteric ischemia may also have intestinal dysbiosis, which can resolve postoperatively.
“A recent study demonstrated that patients with chronic mesenteric ischemia may also have intestinal dysbiosis, which can resolve postoperatively [10].”
From Revascularization Strategies for Acute and Chronic Mesenteric Ischemia: A Narrative Review (2024) · cites this paper as [10]
Adequate intestinal perfusion is important for gut homeostasis and microbiome modulation.
“This study underscores the importance of adequate intestinal perfusion for gut homeostasis and microbiome modulation [10].”
From Revascularization Strategies for Acute and Chronic Mesenteric Ischemia: A Narrative Review (2024) · cites this paper as [10]
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DADA2: High–resolution sample inference from Illumina amplicon data
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016) · Nature Methods · doi:10.1038/nmeth.3869 · Cited by 35,698 · see citing works
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0209-9 · Cited by 23,742 · see citing works
Metagenomic biomarker discovery and explanation
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W. S., & Huttenhower, C. (2011) · Genome Biology · doi:10.1186/gb-2011-12-6-r60 · Cited by 16,192 · see citing works
Bokulich, N. A., Kaehler, B. D., Rideout, J. R., Dillon, M. R., Bolyen, E. K., Knight, R. D., Huttley, G. A., & Caporaso, J. G. (2018) · Microbiome · doi:10.1186/s40168-018-0470-z · Cited by 5,873 · see citing works
Gupta, V. K., Paul, S., & Dutta, C. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01162 · Cited by 1,019 · see citing works
Insights into the Role of Erysipelotrichaceae in the Human Host
Kaakoush, N. O. (2015) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2015.00084 · Cited by 817 · see citing works
Commensal clostridia: Leading players in the maintenance of gut homeostasis
Lopetuso, L. R., Scaldaferri, F., Petito, V., & Gasbarrini, A. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-23 · Cited by 753 · see citing works
The role of diet on gut microbiota composition.
Bibbò, S., Ianiro, G., Giorgio, V., Scaldaferri, F., Masucci, L., Gasbarrini, A., & Cammarota, G. (2016) · PubMed · Cited by 358 · see citing works
Antibiotic use and microbiome function
Ferrer, M., Méndez–García, C., Rojo, D., Barbas, C., & Moyá, A. (2016) · Biochemical Pharmacology · doi:10.1016/j.bcp.2016.09.007 · Cited by 300 · see citing works
Microbiota succession throughout life from the cradle to the grave
Martino, C., Dilmore, A. H., Burcham, Z. M., Metcalf, J. L., Jeste, D., & Knight, R. (2022) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00768-z · Cited by 275 · see citing works
Belizário, J. E., & Faintuch, J. (2018) · Experientia supplementum · doi:10.1007/978-3-319-74932-7_13 · Cited by 265 · see citing works
Hu, J., Deng, F., Zhao, B.-C., Lin, Z., Sun, Q., Yang, X. Y., Wu, M., Qiu, S.-D., Chen, Y., Yan, Z., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01227-w · Cited by 249 · see citing works
The essential role of the intestinal microbiota in facilitating acute inflammatory responses
Souza, D. G., Vieira, A. T., Soares, A. C., Pinho, V., Nicoli, J. R., Vieira, L. Q., & Teixeira, M. M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.6.4137 · Cited by 247 · see citing works
Saccon, T. D., Nagpal, R., Yadav, H., Cavalcante, M. B., Nunes, A. D. D. C., Schneider, A., Gesing, A., Hughes, B., Yousefzadeh, M., Tchkonia, T., et al. (2021) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glab002 · Cited by 247 · see citing works
Self-citationDeng, F., Zhao, B.-C., Yang, X. Y., Lin, Z., Sun, Q., Wang, Y., Yan, Z., Liu, W.-F., Li, C., Hu, J., et al. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1902719 · Cited by 246 · see citing works
Bui, T. P. N., Mannerås-Holm, L., Puschmann, R., Wu, H., Troise, A. D., Nijsse, B., Boeren, S. A., Bäckhed, F., Fiedler, D., & de Vos, W. M. (2021) · Nature Communications · doi:10.1038/s41467-021-25081-w · Cited by 223 · see citing works
From correlation to causality: the case of Subdoligranulum
Hul, M. V., Roy, T. L., Prifti, E., Dao, M. C., Paquot, A., Zucker, J., Delzenne, N. M., Muccioli, G. G., Clément, K., & Cani, P. D. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1849998 · Cited by 221 · see citing works
ACR appropriateness criteria® imaging of mesenteric ischemia
Oliva, I. B., Davarpanah, A. H., Rybicki, F. J., Desjardins, B., Flamm, S. D., Francois, C. J., Gerhard-Herman, M. D., Kalva, S. P., Ashraf Mansour, M., Mohler, E. R., et al. (2013) · Abdominal Imaging · doi:10.1007/s00261-012-9975-2 · Cited by 200 · see citing works
Human Intestinal Ischemia-Reperfusion–Induced Inflammation Characterized
Grootjans, J., Lenaerts, K., Derikx, J. P. M., Matthijsen, R. A., de Bruïne, A. P., van Bijnen, A. A., van Dam, R. M., Dejong, C. H. C., & Buurman, W. A. (2010) · The American Journal of Pathology · doi:10.2353/ajpath.2010.091069 · Cited by 186 · see citing works
The Gut Microbiome and Sex Hormone-Related Diseases
He, S., Li, H., Yu, Z., Zhang, F., Liang, S., Liu, H., Chen, H., & Lü, M. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.711137 · Cited by 176 · see citing works
Gut integrity in critical illness
Otani, S., & Coopersmith, C. M. (2019) · Journal of Intensive Care · doi:10.1186/s40560-019-0372-6 · Cited by 165 · see citing works
Chronic mesenteric ischemia: Clinical practice guidelines from the Society for Vascular Surgery
Huber, T. S., Björck, M., Chandra, A., Clouse, W. D., Dalsing, M. C., Oderich, G. S., Smeds, M. R., & Murad, M. H. (2021) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2020.10.029 · Cited by 152 · see citing works
Derikx, J. P. M., Matthijsen, R. A., A, A. P. D. B., van Bijnen, A. A. J. H. M., Heineman, E., van Dam, R. M., Dejong, C. H. C., & Buurman, W. A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003428 · Cited by 126 · see citing works
Alahdab, F., Arwani, R., Pasha, A. K., Razouki, Z. A., Prokop, L. J., Huber, T. S., & Murad, M. H. (2018) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2017.12.046 · Cited by 114 · cited 2× · see citing works
“CMI is a devastating disease for which the standard of care with open or endovascular mesenteric revascularization can result in systemic inflammation and a morbid postoperative course.(2,3) In our study, we found that CMI induces intestinal dysbiosis, characterized by decreased alpha-diversity and a unique microbial…”
Depletion of gut commensal bacteria attenuates intestinal ischemia/reperfusion injury
Yoshiya, K., Lapchak, P. H., Thai, T., Kannan, L., Rani, P., Lucca, J. J. D., & Tsokos, G. C. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00239.2011 · Cited by 101 · see citing works
ACR appropriateness criteria® imaging of mesenteric ischemia
Ginsburg, M., Obara, P., Lambert, D. L., Hanley, M., Steigner, M. L., Camacho, M. A., Chandra, A., Chang, K. J., Gage, K. L., Peterson, C. M., et al. (2018) · Journal of the American College of Radiology · doi:10.1016/j.jacr.2018.09.018 · Cited by 99 · see citing works
Dynamic Alteration of the Colonic Microbiota in Intestinal Ischemia-Reperfusion Injury
Wang, F., Li, Q., Wang, C., Tang, C. X., & Li, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042027 · Cited by 92 · see citing works
Kaur, S., Yawar, M., Kumar, P. A., & Suresh, K. N. (2013) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.056986-0 · Cited by 76 · see citing works
Mikami, A., Ogita, T., Namai, F., Shigemori, S., Sato, T., & Shimosato, T. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2020.610946 · Cited by 70 · see citing works
Serum D-lactate levels as a predictor of intestinal ischemia-reperfusion injury
Günel, E., Çağlayan, O., & Çağlayan, F. (1998) · Pediatric Surgery International · doi:10.1007/s003830050436 · Cited by 56 · see citing works
Temporal Variations of the Ileal Microbiota in Intestinal Ischemia and Reperfusion
Wang, F., Li, Q., He, Q., Geng, Y., Tang, C., Wang, C., & Li, J. (2012) · Shock · doi:10.1097/shk.0b013e318279265f · Cited by 48 · see citing works
Deng, F., Hu, J., Yang, X. Y., Sun, Q., Lin, Z., Zhao, B.-C., Yao, Z., Luo, S.-D., Chen, Z.-L., Liu, Y., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.704836 · Cited by 47 · see citing works
Intestinal diamine oxidase levels reflect ischemic injury
Bragg, L. E., Thompson, J. S., & West, W. W. (1991) · Journal of Surgical Research · doi:10.1016/0022-4804(91)90183-m · Cited by 46 · see citing works
Association of Gut Microbiota With Intestinal Ischemia/Reperfusion Injury
Chen, J., Wang, Y. H. D., Shi, Y., Liu, Y., Wu, C., & Luo, Y. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.962782 · Cited by 37 · see citing works
Wang, B., Huang, Q., Zhang, W., Li, N., & Li, J. (2011) · Digestive Diseases and Sciences · doi:10.1007/s10620-011-1747-2 · Cited by 36 · see citing works
Ischemia/Reperfusion Injury Alters Sphingolipid Metabolism in the Gut
Hoehn, R. S., Seitz, A. P., Jernigan, P. L., Gulbins, E., & Edwards, M. J. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000447831 · Cited by 35 · see citing works
Zhang, X., Liu, Z., Zhang, H., Li, Y., Wen, S., Shen, J., Huang, W., & Liu, K. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12789 · Cited by 34 · see citing works
The Impact of a Mediterranean Diet on the Gut Microbiome in Healthy Human Subjects: A Pilot Study
Rejeski, J., Wilson, F. M., Nagpal, R., Yadav, H., & Weinberg, R. B. (2021) · Digestion · doi:10.1159/000519445 · Cited by 34 · see citing works
Self-citationProtective effects of butyrate on intestinal ischemia–reperfusion injury in rats
Qiao, Y., Qian, J., Lu, Q., Tian, Y., Chen, Q., & Zhang, Y. (2015) · Journal of Surgical Research · doi:10.1016/j.jss.2015.04.031 · Cited by 32 · see citing works
Collange, O., Tamion, F., Chanel, S., et al. (2006) · Critical Care Medicine · doi:10.1097/01.ccm.0000214517.24064.35 · Cited by 30 · see citing works
Bifidobacterium bifidum PRL2010 alleviates intestinal ischemia/reperfusion injury
Duranti, S., Vivo, V., Zini, I., Milani, C., Mangifesta, M., Anzalone, R., Mancabelli, L., Viappiani, A., Cantoni, A. M., Barocelli, E., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0202670 · Cited by 29 · see citing works
The microbiome and the immune system in critical illness
Miniet, A. A., Grunwell, J. R., & Coopersmith, C. M. (2021) · Current Opinion in Critical Care · doi:10.1097/mcc.0000000000000800 · Cited by 27 · see citing works
Huang, W., Yan, Y., Wu, M., Hu, J., Zhao, J., Chen, X., Liu, W., Liu, K., & Li, C. (2021) · British Journal of Anaesthesia · doi:10.1016/j.bja.2021.11.025 · Cited by 27 · see citing works
Antioxidant-Based Therapy Reduces Early-Stage Intestinal Ischemia-Reperfusion Injury in Rats
Gutiérrez-Sánchez, G., Garcı́a-Alonso, I., María, J. G. S. D. S., Alonso‐Varona, A., & de la Parte, B. H. (2021) · Antioxidants · doi:10.3390/antiox10060853 · Cited by 25 · see citing works
de Aguilar‐Nascimento, J. E., Salomão, A. B., Nochi, R. J., Nascimento, M., & Neves, J. D. S. (2006) · Acta Cirúrgica Brasileira · doi:10.1590/s0102-86502006000100006 · Cited by 23 · see citing works
Schofield, Z., Wu, M. C. L., Hansbro, P. M., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000960r · Cited by 14 · see citing works
Intestinal Microbiome, Akkermansia muciniphila, and Medical Nutrition Therapy.
Bland, J. K. S. (2016) · PubMed Central · Cited by 11 · see citing works
Infections due to Citrobacter and Enterobacter☆
Kus, J. V. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.05089-3 · Cited by 10 · see citing works
Crawford, J. D., Scali, S. T., Khan, T., Back, M. R., Cooper, M. A., Arnaoutakis, D. K., Berceli, S. A., Upchurch, G. R., Huber, T. S., & Giles, K. A. (2021) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2021.03.039 · Cited by 8 · see citing works
Self-citationDual roles of commensal bacteria after intestinal ischemia and reperfusion
Zhang, H., Wang, F., Chen, X., et al. (2019) · Pediatric Surgery International · doi:10.1007/s00383-019-04555-5 · Cited by 3 · see citing works
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Revascularization Strategies for Acute and Chronic Mesenteric Ischemia: A Narrative Review
Gries, J. J., Sakamoto, T., Chen, B., Virk, H. U. H., Alam, M., & Krittanawong, C. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13051217 · Cited by 19 · see citing works
“This study underscores the importance of adequate intestinal perfusion for gut homeostasis and microbiome modulation [10].”
Background
- Authors
- Munley, J. A., Nagpal, R., Hanson, N. C., Mirzaie, A., Laquian, L., Mohr, A. M., Efron, P. A., Arnaoutakis, D. J., & Cooper, M. A.
- Affiliations
- University of Florida Health (US)
- Florida State University (US)
- University of South Florida (US)
- Corresponding author
- Cooper, Michol A.
- ORCID
- Venue
- Journal of Vascular Surgery Cases, Innovations and Techniques
- Publisher
- Elsevier BV
- Published
- 2023-06
- Volume
- 9
- Issue
- 2
- Pages
- 101084
- ISSN
- 2352-667X (ISSN-L)
- 2468-4287
- PMC
- PMC10033993
- OpenAlex
- W4312157401
- Cited by
- 8
- References
- 50
- Citations by year
- 2025: 2 · 2024: 5 · 2023: 1
- FWCI
- 1.91
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Vascular Surgery Cases and Innovative Techniques (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (T32 GM-008721)
- National Institute of General Medical Sciences
- Topics
- Health Sciences › Medicine › Surgery › Abdominal vascular conditions and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- chronic mesenteric ischemia, gut dysbiosis, gut microbiota, mesenteric revascularization, alpha diversity, beta diversity, Bacteroidetes, Clostridia, intestinal perfusion, intestinal homeostasis, ischemia-reperfusion injury, postoperative recovery, inflammation, 16S rRNA gene sequencing
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