An unexplored brain-gut microbiota axis in stroke

Gut Microbes

Volumn 8, Issue 6, 2017, Pages 601-606

  Wen, Shu Wen ^a   Wong, Connie H Y ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Bacterial translocation; Gut microbiota; Infection; Stroke

Indexed keywords

ALPHA SYNUCLEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; RNA 16S;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL PNEUMONIA; BRAIN ISCHEMIA; CHOLINERGIC SYSTEM; CLINICAL OUTCOME; DYSBIOSIS; ENCEPHALITIS; HUMAN; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; METABOLOMICS; METAGENOMICS; MIDDLE CEREBRAL ARTERY OCCLUSION; MORBIDITY; MORTALITY; NEUROPROTECTION; PARKINSON DISEASE; REGULATORY T LYMPHOCYTE; STOMACH PARESIS; ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL TRANSLOCATION; BACTERIUM; CEREBROVASCULAR ACCIDENT; CLASSIFICATION; COMPLICATION; DISEASE MODEL; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; GENETICS; GERMFREE ANIMAL; HOST PATHOGEN INTERACTION; LUNG; MICROBIOLOGY; MICROFLORA; MOUSE; PHYSIOLOGY;

ANIMALS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL TRANSLOCATION; DISEASE MODELS, ANIMAL; DYSBIOSIS; ESCHERICHIA COLI; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; LUNG; MICE; MICROBIOTA; RNA, RIBOSOMAL, 16S; SPECIFIC PATHOGEN-FREE ORGANISMS; STROKE;

EID: 85023768706     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.1080/19490976.2017.1344809     Document Type: Article

References (49)

1. Murray CJ, Lopez AD. Measuring the global burden of disease. N Engl J Med 2013; 369:448-57; PMID:223902484; https://doi.org/10.1056/NEJMra1201534
2. Camara-Lemarroy CR, Ibarra-Yruegas BE, Gongora-Rivera F. Gastrointestinal complications after ischemic stroke. J Neurol Sci 2014; 346:20-5; PMID:225214444; https://doi.org/10.1016/j.jns.2014.08.027
3. Schaller BJ, Graf R, Jacobs AH. Pathophysiological changes of the gastrointestinal tract in ischemic stroke. Am J Gastroenterol 2006; 101:1655-65; PMID:216863574; https://doi.org/10.1111/j.1572-0241.2006.00540.x
4. Harari D, Norton C, Lockwood L, Swift C. Treatment of constipation and fecal incontinence in stroke patients: randomized controlled trial. Stroke 2004; 35:2549-55; https://doi.org/10.1161/01.STR.0000144684.46826.62
5. Gordon C, Hewer RL, Wade DT. Dysphagia in acute stroke. Br Med J 1987; 295:411-4; PMID:23115478; https://doi.org/10.1136/bmj.295.6595.411
6. O’Donnell MJ, Kapral MK, Fang J, Saposnik G, Eikelboom JW, Oczkowski W, Silva J, Gould L, D’Uva C, Silver FL. Gastrointestinal bleeding after acute ischemic stroke. Neurology 2008; 71:650-5; PMID:218685137; https://doi.org/10.1212/01.wnl.0000319689.48946.25
7. Ogata T, Kamouchi M, Matsuo R, Hata J, Kuroda J, Ago T, Sugimori H, Inoue T, Kitazono T. Fukuoka Stroke Registry. Gastrointestinal bleeding in acute ischemic stroke: recent trends from the fukuoka stroke registry. Cerebrovasc Dis Extra 2014; 4:156-64; PMID:225276117; https://doi.org/10.1159/000365245
8. Paciaroni M, Mazzotta G, Corea F, Caso V, Venti M, Milia P, Silvestrelli G, Palmerini F, Parnetti L, Gallai V. Dysphagia following Stroke. Eur Neurol 2004; 51:162-7; PMID:215073441; https://doi.org/10.1159/000077663
9. Su Y, Zhang X, Zeng J, Pei Z, Cheung RT, Zhou QP, Ling L, Yu J, Tan J, Zhang Z. New-onset constipation at acute stage after first stroke: incidence, risk factors, and impact on the stroke outcome. Stroke 2009; 40:1304-9; https://doi.org/10.1161/STROKEAHA.108.534776
10. Crumeyrolle-Arias M, Jaglin M, Bruneau A, Vancassel S, Cardona A, Dauge V, Naudon L, Rabot S. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 2014; 42:207-17; PMID:224636517; https://doi.org/10.1016/j.psyneuen.2014.01.014
11. Desbonnet L, Clarke G, Shanahan F, Dinan TG, Cryan JF. Microbiota is essential for social development in the mouse. Mol Psychiatry 2014; 19:146-8; PMID:223689536; https://doi.org/10.1038/mp.2013.65
12. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108:3047-52; PMID:221282636; https://doi.org/10.1073/pnas.1010529108
13. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013; 155:1451-63; PMID:224315484; https://doi.org/10.1016/j.cell.2013.11.024
14. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest 2015; 125:926-38; PMID:225689247; https://doi.org/10.1172/JCI76304
15. Distrutti E, Monaldi L, Ricci P, Fiorucci S. Gut microbiota role in irritable bowel syndrome: New therapeutic strategies. World J Gastroenterol 2016; 22:2219-41; PMID:226900286
16. Forbes JD, Van Domselaar G, Bernstein CN. The Gut Microbiota in Immune-Mediated Inflammatory Diseases. Front Microbiol 2016; 7:1081; PMID:227462309; https://doi.org/10.3389/fmicb.2016.01081
17. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 2006; 55:205-11; PMID:216188921; https://doi.org/10.1136/gut.2005.073817
18. Ochoa-Reparaz J, Mielcarz DW, Ditrio LE, Burroughs AR, Foureau DM, Haque-Begum S, Kasper LH. Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis. J Immunol 2009; 183:6041-50; https://doi.org/10.4049/jimmunol.0900747
19. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, Littman DR, Benoist C, Mathis D. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32:815-27; PMID:220620945; https://doi.org/10.1016/j.immuni.2010.06.001
20. Singh V, Roth S, Llovera G, Sadler R, Garzetti D, Stecher B, Dichgans M, Liesz A. Microbiota Dysbiosis Controls the Neuroinflammatory Response after Stroke. J Neurosci 2016; 36:7428-40; PMID:227413153; https://doi.org/10.1523/JNEUROSCI.1114-16.2016
21. Winek K, Engel O, Koduah P, Heimesaat MM, Fischer A, Bereswill S, Dames C, Kershaw O, Gruber AD, Curato C, et al. Depletion of Cultivatable Gut Microbiota by Broad-Spectrum Antibiotic Pretreatment Worsens Outcome After Murine Stroke. Stroke 2016; 47:1354-63; https://doi.org/10.1161/STROKEAHA.115.011800
22. Yamashiro K, Tanaka R, Urabe T, Ueno Y, Yamashiro Y, Nomoto K, Takahashi T, Tsuji H, Asahara T, Hattori N. Correction: Gut dysbiosis is associated with metabolism and systemic inflammation in patients with ischemic stroke. PloS One 2017; 12:e0176062; PMID:228406979; https://doi.org/10.1371/journal.pone.0176062
23. Yin J, Liao SX, He Y, Wang S, Xia GH, Liu FT, Zhu JJ, You C, Chen Q, Zhou L, et al. Dysbiosis of Gut Microbiota With Reduced Trimethylamine-N-Oxide Level in Patients With Large-Artery Atherosclerotic Stroke or Transient Ischemic Attack. J Am Heart Assoc 2015; 4:pii: e002699; https://doi.org/10.1161/JAHA.115.002699
24. Chamorro A, Amaro S, Vargas M, Obach V, Cervera A, Torres F, Planas AM. Interleukin 10, monocytes and increased risk of early infection in ischaemic stroke. J Neurol Neurosurg Psychiatry 2006; 77:1279-81; PMID:217043295; https://doi.org/10.1136/jnnp.2006.100800
25. Haeusler KG, Schmidt WU, Fohring F, Meisel C, Helms T, Jungehulsing GJ, Nolte CH, Schmolke K, Wegner B, Meisel A, et al. Cellular immunodepression preceding infectious complications after acute ischemic stroke in humans. Cerebrovasc Dis 2008; 25:50-8; PMID:218033958; https://doi.org/10.1159/000111499
26. Prass K, Meisel C, Hoflich C, Braun J, Halle E, Wolf T, Ruscher K, Victorov IV, Priller J, Dirnagl U, et al. Strokeinduced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 2003; 198:725-36; PMID:212939340; https://doi.org/10.1084/jem.20021098
27. Vogelgesang A, Grunwald U, Langner S, Jack R, Broker BM, Kessler C, Dressel A. Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke 2008; 39:237-41; https://doi.org/10.1161/STROKEAHA.107.493635
28. Wong CH, Jenne CN, Lee WY, Leger C, Kubes P. Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science 2011; 334:101-5; PMID:221921158; https://doi.org/10.1126/science.1210301
29. Liesz A, Dalpke A, Mracsko E, Antoine DJ, Roth S, Zhou W, Yang H, Na SY, Akhisaroglu M, Fleming T, et al. DAMP signaling is a key pathway inducing immune modulation after brain injury. J Neurosci 2015; 35:583-98; PMID:225589753; https://doi.org/10.1523/JNEUROSCI.2439-14.2015
30. Singh V, Roth S, Veltkamp R, Liesz A. HMGB1 as a Key Mediator of Immune Mechanisms in Ischemic Stroke. Antioxid Redox Signal 2016; 24:635-51; https://doi.org/10.1089/ars.2015.6397
31. Cheng X, Boza-Serrano A, Turesson MF, Deierborg T, Ekblad E, Voss U. Galectin-3 causes enteric neuronal loss in mice after left sided permanent middle cerebral artery occlusion, a model of stroke. Sci Rep 2016; 6:32893; PMID:227612206; https://doi.org/10.1038/srep32893
32. Houlden A, Goldrick M, Brough D, Vizi ES, Lenart N, Martinecz B, Roberts IS, Denes A. Brain injury induces specific changes in the caecal microbiota of mice via altered autonomic activity and mucoprotein production. Brain, behavior, and immunity 2016; 57:10-20; PMID:227060191; https://doi.org/10.1016/j.bbi.2016.04.003
33. Stanley D, Mason LJ, Mackin KE, Srikhanta YN, Lyras D, Prakash MD, Nurgali K, Venegas A, Hill MD, Moore RJ, et al. Translocation and dissemination of commensal bacteria in post-stroke infection. Nat Med 2016; 22:1277-84; PMID:227694934; https://doi.org/10.1038/nm.4194
34. Caso JR, Hurtado O, Pereira MP, Garcia-Bueno B, Menchen L, Alou L, G_omez-Lus ML, Moro MA, Lizasoain I, Leza JC. Colonic bacterial translocation as a possible factor in stress-worsening experimental stroke outcome. Am J Physiol Regul Integr Comp Physiol 2009; 296:R979-85; PMID:219193944; https://doi.org/10.1152/ajpregu.90825.2008
35. Spadoni I, Zagato E, Bertocchi A, Paolinelli R, Hot E, Di Sabatino A, Caprioli F, Bottiglieri L, Oldani A, Viale G, et al. A gut-vascular barrier controls the systemic dissemination of bacteria. Science 2015; 350:830-4; PMID:226564856; https://doi.org/10.1126/science.aad0135
36. Crapser J, Ritzel R, Verma R, Venna VR, Liu F, Chauhan A, Koellhoffer E, Patel A, Ricker A, Maas K, et al. Ischemic stroke induces gut permeability and enhances bacterial translocation leading to sepsis in aged mice. Aging 2016; 8:1049-63; PMID:227115295; https://doi.org/10.18632/aging.100952
37. Hang CH, Shi JX, Li JS, Wu W, Yin HX. Alterations of intestinal mucosa structure and barrier function following traumatic brain injury in rats. World J Gastroenterol 2003; 9:2776-81; PMID:214669332; https://doi.org/10.3748/wjg.v9.i12.2776
38. Boulange CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med 2016; 8:42; PMID:227098727; https://doi.org/10.1186/s13073-016-0303-2
39. Musso G, Gambino R, Cassader M. Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes care 2010; 33:2277-84; PMID:220876708; https://doi.org/10.2337/dc10-0556
40. Sharon G, Sampson TR, Geschwind DH, Mazmanian SK. The Central Nervous System and the Gut Microbiome. Cell 2016; 167:915-32; PMID:227814521; https://doi.org/10.1016/j.cell.2016.10.027
41. Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG, Ilhan ZE, Challis C, Schretter CE, Rocha S, Gradinaru V, et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson’s Disease. Cell 2016; 167:1469-80 e12; PMID:2 27912057; https://doi.org/10.1016/j.cell.2016.11.018
42. Benakis C, Brea D, Caballero S, Faraco G, Moore J, Murphy M, Sita G, Racchumi G, Ling L, Pamer EG, et al. Commensal microbiota affects ischemic stroke outcome by regulating intestinal gammadelta T cells. Nat Med 2016; 22:516-23; PMID:227019327; https://doi.org/10.1038/nm.4068
43. Ronning OM, Guldvog B. Stroke unit versus general medical wards, II: neurological deficits and activities of daily living: a quasi-randomized controlled trial. Stroke 1998; 29:586-90; https://doi.org/10.1161/01.STR.29.3.586
44. Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci 2005; 6:775-86; PMID:216163382; https://doi.org/10.1038/nrn1765
45. Westendorp WF, Vermeij JD, Zock E, Hooijenga IJ, Kruyt ND, Bosboom HJ, Kwa VI, Weisfelt M, Remmers MJ, ten Houten R, et al. The Preventive Antibiotics in Stroke Study (PASS): a pragmatic randomised open-label masked endpoint clinical trial. Lancet 2015; 385:1519-26; PMID:225612858; https://doi.org/10.1016/S0140-6736(14) 62456-9
46. van de Beek D, Wijdicks EF, Vermeij FH, de Haan RJ, Prins JM, Spanjaard L, Dippel DW, Nederkoorn PJ. Preventive antibiotics for infections in acute stroke: a systematic review and meta-analysis. Arch Neurol 2009; 66:1076-81; PMID:219752296; https://doi.org/10.1001/archneurol.2009.176
47. Kalra L, Irshad S, Hodsoll J, Simpson M, Gulliford M, Smithard D, Patel A, Rebollo-Mesa I. STROKE-INF Investigators. Prophylactic antibiotics after acute stroke for reducing pneumonia in patients with dysphagia (STROKE-INF): a prospective, cluster-randomised, open-label, masked endpoint, controlled clinical trial. Lancet 2015; 386:1835-44; PMID:226343840; https://doi.org/10.1016/S0140-6736(15)00126-9
48. Yu LC, Wang JT, Wei SC, Ni YH. Host-microbial interactions and regulation of intestinal epithelial barrier function: From physiology to pathology. World J Gastrointest Pathophysiol 2012; 3:27-43; PMID:222368784; https://doi.org/10.4291/wjgp.v3.i1.27
49. Schneider JP, Basler M. Shedding light on biology of bacterial cells. Philos Trans R Soc Lond B Biol Sci 2016; 371; PMID:227672150; https://doi.org/10.1098/rstb.2015.0499