Gut microbiota changes in animal models of spinal cord injury: a preclinical systematic review and meta-analysis

References

• Chen J, Wang Z, Mao Y, et al. Liraglutide activates autophagy via GLP-1R to improve functional recovery after spinal cord injury. Oncotarget. 2017;8(49):1–16. doi: 10.18632/oncotarget.20791.
   PubMedGoogle Scholar
• Ma K, Xu H, Zhang J, et al. Insulin-like growth factor-1 enhances neuroprotective effects of neural stem cell exosomes after spinal cord injury via an miR-219a-2-3p/YY1 mechanism. Aging. 2019;11(24):12278–12294. doi: 10.18632/aging.102568.
   PubMedGoogle Scholar
• Singh A, Tetreault L, Kalsi-Ryan S, et al. Global prevalence and incidence of traumatic spinal cord injury. Clin Epidemiol. 2014;6:309–331. doi: 10.2147/CLEP.S68889.
   PubMed Web of Science ®Google Scholar
• Zhang T, Li K, Zhang ZL, et al. LncRNA Airsci increases the inflammatory response after spinal cord injury in rats through the nuclear factor kappa B signaling pathway. Neural Regen Res. 2021;16(4):772–777. doi: 10.4103/1673-5374.295335.
   PubMed Web of Science ®Google Scholar
• Li HX, Cui J, Fan JS, et al. An observation of the clinical efficacy of combining Riluzole with mannitol and hyperbaric oxygen in treating acute spinal cord injury. Pak J Med Sci. 2021;37(2):320–324. doi: 10.12669/pjms.37.2.3418.
   PubMed Web of Science ®Google Scholar
• Huang Z, Gong J, Lin W, et al. Catalpol as a component of rehmannia glutinosa protects spinal cord injury by inhibiting endoplasmic reticulum stress-mediated neuronal apoptosis. Front Pharmacol. 2022;13:860757. doi: 10.3389/fphar.2022.860757.
   PubMed Web of Science ®Google Scholar
• Zou HJ, Guo SW, Zhu L, et al. Methylprednisolone induces neuro-protective effects via the inhibition of A1 astrocyte activation in traumatic spinal cord injury mouse models. Front Neurosci. 2021;15:628917. doi: 10.3389/fnins.2021.628917.
   PubMed Web of Science ®Google Scholar
• Vaughn BP, Rank KM, Khoruts A. Fecal microbiota transplantation: current status in treatment of GI and liver disease. Clin Gastroenterol Hepatol. 2019;17(2):353–361. doi: 10.1016/j.cgh.2018.07.026.
   PubMed Web of Science ®Google Scholar
• Evrensel A, Ceylan ME. Fecal microbiota transplantation and its usage in neuropsychiatric disorders. Clin Psychopharmacol Neurosci. 2016;14(3):231–237. doi: 10.9758/cpn.2016.14.3.231.
   PubMed Web of Science ®Google Scholar
• Tkach S, Dorofeyev A, Kuzenko I, et al. Current status and future therapeutic options for fecal microbiota transplantation. Medicina. 2022;58(1):84. doi: 10.3390/medicina58010084.
   PubMed Web of Science ®Google Scholar
• Yuan B, Lu XJ, Wu Q. Gut microbiota and acute Central nervous system injury: a new target for therapeutic intervention. Front Immunol. 2021;12:800796. doi: 10.3389/fimmu.2021.800796.
   PubMed Web of Science ®Google Scholar
• Zheng Z, Wang S, Wu C, et al. Gut microbiota dysbiosis after traumatic brain injury contributes to persistent microglial activation associated with upregulated Lyz2 and shifted tryptophan metabolic phenotype. Nutrients. 2022;14(17):3467. doi: 10.3390/nu14173467.
   PubMed Web of Science ®Google Scholar
• Mayer EA, Nance K, Chen S. The Gut-Brain axis. Annu Rev Med. 2022;73(1):439–453. doi: 10.1146/annurev-med-042320-014032.
   PubMedGoogle Scholar
• Dalile B, Van Oudenhove L, Vervliet B, et al. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat Rev Gastroenterol Hepatol. 2019;16(8):461–478. doi: 10.1038/s41575-019-0157-3.
   PubMed Web of Science ®Google Scholar
• Bannerman CA, Douchant K, Sheth PM, et al. The gut-brain axis and beyond: microbiome control of spinal cord injury pain in humans and rodents. Neurobiol Pain. 2021;9:100059. doi: 10.1016/j.ynpai.2020.100059.
   PubMedGoogle Scholar
• Qi Z, Middleton JW, Malcolm A. Bowel dysfunction in spinal cord injury. Curr Gastroenterol Rep. 2018;20(10):47. doi: 10.1007/s11894-018-0655-4.
   PubMedGoogle Scholar
• Liu X, Liu N, Zhou M, et al. Bibliometric analysis of global research on the rehabilitation of spinal cord injury in the past two decades. Ther Clin Risk Manag. 2019;15:1–14. doi: 10.2147/TCRM.S163881.
   PubMed Web of Science ®Google Scholar
• Jing Y, Bai F, Wang L, et al. Fecal microbiota transplantation exerts neuroprotective effects in a mouse spinal cord injury model by modulating the microenvironment at the lesion site. Microbiol Spectr. 2022;10(3):e0017722. doi: 10.1128/spectrum.00177-22.
   PubMed Web of Science ®Google Scholar
• Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg. 2021;88:105906. doi: 10.1016/j.ijsu.2021.105906.
   PubMed Web of Science ®Google Scholar
• Haining L, Hao W, Can Y, et al. Advanced methods of data extraction for continuous outcomes in meta-analysis. Chin J Evid Based Med. 2017;17:117–121. doi: 10.7507/1672-2531.201612004.
   Google Scholar
• Higgins JP, Altman DG, Gøtzsche PC, et al. The cochrane collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343(2):d5928–d5928. doi: 10.1136/bmj.d5928.
   PubMed Web of Science ®Google Scholar
• Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5(1):13. doi: 10.1186/1471-2288-5-13.
   PubMedGoogle Scholar
• Smith AM, Welch BA, Harris KK, et al. Nutrient composition influences the gut microbiota in chronic thoracic spinal cord-injured rats. Physiol Genomics. 2022;54(10):402–415. doi: 10.1152/physiolgenomics.00037.2022.
   PubMed Web of Science ®Google Scholar
• Cheng J, Li W, Wang Y, et al. Electroacupuncture modulates the intestinal microecology to improve intestinal motility in spinal cord injury rats. Microb Biotechnol. 2022;15(3):862–873. doi: 10.1111/1751-7915.13968.
   PubMed Web of Science ®Google Scholar
• Doelman A, Tigchelaar S, McConeghy B, et al. Characterization of the gut microbiome in a porcine model of thoracic spinal cord injury. BMC Genomics. 2021;22(1):775. doi: 10.1186/s12864-021-07979-3.
   PubMed Web of Science ®Google Scholar
• Du J, Zayed AA, Kigerl KA, et al. Spinal cord injury changes the structure and functional potential of gut bacterial and viral communities. mSystems. 2021;6(3):e01356-20. doi: 10.1128/mSystems.01356-20.
   PubMed Web of Science ®Google Scholar
• He N, Shen G, Jin X, et al. Resveratrol suppresses microglial activation and promotes functional recovery of traumatic spinal cord via improving intestinal microbiota. Pharmacol Res. 2022;183:106377. doi: 10.1016/j.phrs.2022.106377.
   PubMed Web of Science ®Google Scholar
• Jing Y, Yu Y, Bai F, et al. Effect of fecal microbiota transplantation on neurological restoration in a spinal cord injury mouse model: involvement of brain-gut axis. Microbiome. 2021;9(1):59. doi: 10.1186/s40168-021-01007-y.
   PubMed Web of Science ®Google Scholar
• Kang JN, Sun ZF, Li XY, et al. Alterations in gut microbiota are related to metabolite profiles in spinal cord injury. Neural Regen Res. 2023;18(5):1076–1083. doi: 10.4103/1673-5374.355769.
   PubMed Web of Science ®Google Scholar
• Kigerl KA, Hall JC, Wang L, et al. Gut dysbiosis impairs recovery after spinal cord injury. J Exp Med. 2016;213(12):2603–2620. doi: 10.1084/jem.20151345.
   PubMed Web of Science ®Google Scholar
• O'Connor G, Jeffrey E, Madorma D, et al. Investigation of microbiota alterations and intestinal inflammation post-spinal cord injury in rat model. J Neurotrauma. 2018;35(18):2159–2166. doi: 10.1089/neu.2017.5349.
   PubMed Web of Science ®Google Scholar
• Rong Z, Huang Y, Cai H, et al. Gut microbiota disorders promote inflammation and aggravate spinal cord injury through the TLR4/MyD88 signaling pathway. Front Nutr. 2021;8:702659. doi: 10.3389/fnut.2021.702659.
   PubMed Web of Science ®Google Scholar
• Rong ZJ, Cai HH, Wang H, et al. Ursolic acid ameliorates spinal cord injury in mice by regulating gut microbiota and metabolic changes. Front Cell Neurosci. 2022;16:872935. doi: 10.3389/fncel.2022.872935.
   PubMed Web of Science ®Google Scholar
• Schmidt EKA, Torres-Espin A, Raposo PJF, et al. Fecal transplant prevents gut dysbiosis and anxiety-like behaviour after spinal cord injury in rats. PLOS One. 2020;15(1):e0226128. doi: 10.1371/journal.pone.0226128.
   PubMed Web of Science ®Google Scholar
• Schmidt EKA, Raposo PJF, Torres-Espin A, et al. Beyond the lesion site: minocycline augments inflammation and anxiety-like behavior following SCI in rats through action on the gut microbiota. J Neuroinflammation. 2021;18(1):144. doi: 10.1186/s12974-021-02123-0.
   PubMed Web of Science ®Google Scholar
• Myers SA, Gobejishvili L, Saraswat Ohri S, et al. Following spinal cord injury, PDE4B drives an acute, local inflammatory response and a chronic, systemic response exacerbated by gut dysbiosis and endotoxemia. Neurobiol Dis. 2019;124:353–363. doi: 10.1016/j.nbd.2018.12.008.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Sui R, Ge L, et al. Moxibustion exhibits therapeutic effects on spinal cord injury via modulating microbiota dysbiosis and macrophage polarization. Aging. 2022;14(14):5800–5811. doi: 10.18632/aging.204184.
   PubMedGoogle Scholar
• Kim BR, Shin J, Guevarra R, et al. Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol. 2017;27(12):2089–2093. doi: 10.4014/jmb.1709.09027.
   PubMed Web of Science ®Google Scholar
• Feranchuk S, Belkova N, Potapova U, et al. Evaluating the use of diversity indices to distinguish between microbial communities with different traits. Res Microbiol. 2018;169(4-5):254–261. doi: 10.1016/j.resmic.2018.03.004.
   PubMed Web of Science ®Google Scholar
• Williams EK, Chang RB, Strochlic DE, et al. Sensory neurons that detect stretch and nutrients in the digestive system. Cell. 2016;166(1):209–221. doi: 10.1016/j.cell.2016.05.011.
   PubMed Web of Science ®Google Scholar
• Margolis KG, Gershon MD, Bogunovic M. Cellular organization of neuroimmune interactions in the gastrointestinal tract. Trends Immunol. 2016;37(7):487–501. doi: 10.1016/j.it.2016.05.003.
   PubMed Web of Science ®Google Scholar
• Bazzocchi G, Turroni S, Bulzamini MC, et al. Changes in gut microbiota in the acute phase after spinal cord injury correlate with severity of the lesion. Sci Rep. 2021;11(1):12743. doi: 10.1038/s41598-021-92027-z.
   PubMed Web of Science ®Google Scholar
• Rodenhouse A, Talukder MAH, Lee JI, et al. Altered gut microbiota composition with antibiotic treatment impairs functional recovery after traumatic peripheral nerve crush injury in mice: effects of probiotics with butyrate producing bacteria. BMC Res Notes. 2022;15(1):80. doi: 10.1186/s13104-022-05967-8.
   PubMed Web of Science ®Google Scholar
• Jing Y, Bai F, Yu Y. Spinal cord injury and gut microbiota: a review. Life Sci. 2021;266:118865. doi: 10.1016/j.lfs.2020.118865.
   PubMed Web of Science ®Google Scholar
• Fengzhi L, Xiaoxin C. Intestinal flora and complications of spinal cord injury. Chin J Microecol. 2020;32(6):741–745. doi: 10.13381/j.carolcarrollnki.CJM.202006026.
   Google Scholar
• Xiaohua Z, Ruihan Z, Wei G, et al. Research progress on the potential effect of intestinal flora on spinal cord injury. Chin J Rehabil Theory Pract. 2019;25(12):1434–1438.
   Google Scholar
• Jogia T, Ruitenberg MJ. Traumatic spinal cord injury and the gut microbiota: current insights and future challenges. Front Immunol. 2020;11:704. doi: 10.3389/fimmu.2020.00704.
   PubMed Web of Science ®Google Scholar
• Hamilton AM, Sampson TR. Traumatic spinal cord injury and the contributions of the post-injury microbiome. Int Rev Neurobiol. 2022;167:251–290. doi: 10.1016/bs.irn.2022.06.003.
   PubMedGoogle Scholar
• Faber W, Stolwijk-Swuste J, van Ginkel F, et al. Faecal microbiota in patients with neurogenic bowel dysfunction and spinal cord injury or multiple sclerosis—a systematic review. J Clin Med. 2021;10(8):1598. doi: 10.3390/jcm10081598.
   PubMed Web of Science ®Google Scholar
• Ding W, You Z, Chen Q, et al. Gut microbiota influences neuropathic pain through modulating proinflammatory and anti-inflammatory T cells. Anesth Analg. 2021;132(4):1146–1155. doi: 10.1213/ANE.0000000000005155.
   PubMed Web of Science ®Google Scholar
• Mazzon C, Zanotti L, Wang L, et al. CCRL2 regulates M1/M2 polarization during EAE recovery phase. J Leukoc Biol. 2016;99(6):1027–1033. doi: 10.1189/jlb.3MA0915-444RR.
   PubMed Web of Science ®Google Scholar
• Jha MK, Lee WH, Suk K. Functional polarization of neuroglia: implications in neuroinflammation and neurological disorders. Biochem Pharmacol. 2016;103:1–16. doi: 10.1016/j.bcp.2015.11.003.
   PubMed Web of Science ®Google Scholar
• Wang H, Liu C, Han M, et al. TRAM1 promotes microglia M1 polarization. J Mol Neurosci. 2016;58(2):287–296. doi: 10.1007/s12031-015-0678-3.
   PubMed Web of Science ®Google Scholar
• Xu S, Zhu W, Shao M, et al. Ecto-5'-nucleotidase (CD73) attenuates inflammation after spinal cord injury by promoting macrophages/microglia M2 polarization in mice. J Neuroinflammation. 2018;15(1):155. doi: 10.1186/s12974-018-1183-8.
   PubMedGoogle Scholar
• Wallace DJ, Sayre NL, Patterson TT, et al. Spinal cord injury and the human microbiome: beyond the brain-gut axis. Neurosurg Focus. 2019;46(3):E11. doi: 10.3171/2018.12.FOCUS18206.
   PubMed Web of Science ®Google Scholar
• Musleh-Vega S, Ojeda J, Vidal PM. Gut Microbiota-Brain axis as a potential modulator of psychological stress after spinal cord injury. Biomedicines. 2022;10(4):847. doi: 10.3390/biomedicines10040847.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Lang R, Guo S, et al. Intestinal microbiota and melatonin in the treatment of secondary injury and complications after spinal cord injury. Front Neurosci. 2022;16:981772. doi: 10.3389/fnins.2022.981772.
   PubMed Web of Science ®Google Scholar
• Kigerl KA, Mostacada K, Popovich PG. Gut microbiota are disease-modifying factors after traumatic spinal cord injury. Neurotherapeutics. 2018;15(1):60–67. doi: 10.1007/s13311-017-0583-2.
   PubMed Web of Science ®Google Scholar
• Blaser MJ. Fecal microbiota transplantation for dysbiosis – predictable risks. N Engl J Med. 2019;381(21):2064–2066. doi: 10.1056/NEJMe1913807.
   PubMed Web of Science ®Google Scholar
• Sanders ME, Merenstein DJ, Reid G, et al. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat Rev Gastroenterol Hepatol. 2019;16(10):605–616. doi: 10.1038/s41575-019-0173-3.
   PubMed Web of Science ®Google Scholar
• Pang R, Wang J, Xiong Y, et al. Relationship between gut microbiota and lymphocyte subsets in Chinese Han patients with spinal cord injury. Front Microbiol. 2022;13:986480. doi: 10.3389/fmicb.2022.986480.
   PubMed Web of Science ®Google Scholar