Posttraumatic stress disorder: Does the gut microbiome hold the key?

Canadian Journal of Psychiatry

Volumn 61, Issue 4, 2016, Pages 204-213

  Leclercq, Sophie ^a,b   Forsythe, Paul ^a,c   Bienenstock, John ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Cortisol; Early life; Gut barrier; Gut microbiota; Immune system; Posttraumatic stress disorders

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE; SEROTONIN;

BEHAVIOR CHANGE; CENTRAL NERVOUS SYSTEM; CLINICAL STUDY; DEPRESSION; DIET; DIGESTION; DISEASE PREDISPOSITION; EARLY LIFE STRESS; ENDOCRINE SYSTEM; FERMENTATION; HOST; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE SYSTEM; INTESTINE FLORA; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PHYSIOLOGICAL PROCESS; POSTTRAUMATIC STRESS DISORDER; PRENATAL PERIOD; REVIEW; IMMUNOLOGY; MICROBIOLOGY;

GASTROINTESTINAL MICROBIOME; HUMANS; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84964058343     PISSN: 07067437     EISSN: 14970015     Source Type: Journal    
DOI: 10.1177/0706743716635535     Document Type: Review

References (111)

1. Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci. 2012;70(1):55-69.
2. Borre YE, O'Keeffe GW, Clarke G, et al. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. 2014;20(9):509-518.
3. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol. 2012;10(11):735-742.
4. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125(3):926-938.
5. Rook GAW, Lowry CA, Raison CL. Microbial "old friends", immunoregulation and stress resilience. Evol Med Public Health. 2013;2013(1):46-64.
6. Bested AC, Logan AC, Selhub EM. Intestinal microbiota, probiotics and mental health: from Metchnikoff to modern advances: Part I - autointoxication revisited. Gut Pathog. 2013;5(1):5.
7. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701-712.
8. Freestone PPE, Sandrini SM, Haigh RD, et al. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol. 2008;16(2):55-64.
9. Olofsson PS, Rosas-Ballina M, Levine YA, et al. Rethinking inflammation: neural circuits in the regulation of immunity. Immunol Rev. 2012;248(1):188-204.
10. Martelli D, McKinley MJ, McAllen RM. The cholinergic anti-inflammatory pathway: a critical review. Auton Neurosci Basic Clin. 2014;182:65-69.
11. Krishnan V, Han M-H, Graham DL, et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell. 2007;131(2):391-404.
12. O'Leary OF, Felice D, Galimberti S, et al. GABAB(1) receptor subunit isoforms differentially regulate stress resilience. Proc Natl Acad Sci U S A. 2014;111(42):15232-15237.
13. Gimeno D, Kivimäki M, Brunner EJ, et al. Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychol Med. 2009;39(03):413-423.
14. Zalli A, Jovanova O, Hoogendijk WJG, et al. Low-grade inflammation predicts persistence of depressive symptoms. Psychopharmacology (Berl). 2015 Apr 16; Epub ahead of print.
15. Dinan TG. Inflammatory markers in depression. Curr Opin Psychiatry. 2009;22(1):32-36.
16. Hodes GE, Pfau ML, Leboeuf M, et al. Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc Natl Acad Sci U S A. 2014;111(45):16136-16141.
17. Eraly SA, Nievergelt CM, Maihofer AX, et al. Assessment of plasma C-reactive protein as a biomarker of posttraumatic stress disorder risk. JAMA Psychiatry. 2014;71(4):423.
18. Rohleder N, Joksimovic L, Wolf JM, et al. Hypocortisolism and increased glucocorticoid sensitivity of pro-inflammatory cytokine production in Bosnian war refugees with posttraumatic stress disorder. Biol Psychiatry. 2004;55(7):745-751.
19. Yehuda R. Post-traumatic stress disorder. N Engl J Med. 2002; 346(2):108-114.
20. Ehring T, Ehlers A, Cleare AJ, et al. Do acute psychological and psychobiological responses to trauma predict subsequent symptom severities of PTSD and depression? Psychiatry Res. 2008;161(1):67-75.
21. McFarlane AC, Barton CA, Yehuda R, et al. Cortisol response to acute trauma and risk of posttraumatic stress disorder. Psychoneuroendocrinology. 2011;36(5):720-727.
22. Pervanidou P. Biology of post-traumatic stress disorder in childhood and adolescence. J Neuroendocrinol. 2008;20(5):632-638.
23. Baumeister D, Akhtar R, Ciufolini S, et al. Childhood trauma and adulthood inflammation: a meta-analysis of peripheral C-reactive protein, interleukin-6 and tumour necrosis factor-α. Mol Psychiatry. 2015 Jun 2; Epub ahead of print.
24. Wiles N, Thomas L, Abel A, et al. Clinical effectiveness and cost-effectiveness of cognitive behavioural therapy as an adjunct to pharmacotherapy for treatment-resistant depression in primary care: the CoBalT randomised controlled trial. Health Technol Assess Winch Engl. 2014;18(31):1-167.
25. Kéri S, Szabó C, Kelemen O. Expression of toll-like receptors in peripheral blood mononuclear cells and response to cognitive-behavioral therapy in major depressive disorder. Brain Behav Immun. 2014;40:235-243.
26. Dantzer R, O'Connor JC, Freund GG, et al. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9:46-56.
27. Maes M. Major depression and activation of the inflammatory response system. Adv Exp Med Biol. 1999;461:25-46.
28. Meyer U, Feldon J, Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res. 2011;69:26R-33R.
29. Duerkop BA, Vaishnava S, Hooper LV. Immune responses to the microbiota at the intestinal mucosal surface. Immunity. 2009;31(3):368-376.
30. Rakoff-Nahoum S, Medzhitov R. Role of the innate immune system and host-commensal mutualism. Curr Top Microbiol Immunol. 2006;308:1-18.
31. Furusawa Y, Obata Y, Fukuda S, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446-450.
32. Söderholm JD, Perdue MH. Stress and gastrointestinal tract. II. Stress and intestinal barrier function. Am J Physiol Gastrointest Liver Physiol. 2001;280(1):G7-13.
33. Saunders PR, Santos J, Hanssen NPM, et al. Physical and psychological stress in rats enhances colonic epithelial permeability via peripheral CRH. Dig Dis Sci. 2002;47(1):208-215.
34. Leclercq S, Cani PD, Neyrinck AM, et al. Role of intestinal permeability and inflammation in the biological and behavioral control of alcohol-dependent subjects. Brain Behav Immun. 2012;26:911-918.
35. Maes M, Kubera M, Leunis J-C, et al. Increased IgA and IgM responses against gut commensals in chronic depression: further evidence for increased bacterial translocation or leaky gut. J Affect Disord. 2012 ;141(1):55-62.
36. Müller N, Schwarz MJ, Dehning S, et al. The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Mol Psychiatry. 2006;11(7):680-684.
37. Kenis G, Maes M. Effects of antidepressants on the production of cytokines. Int J Neuropsychopharmacol. 2002;5(4):401-412.
38. Davey KJ, O'Mahony SM, Schellekens H, et al. Gender-dependent consequences of chronic olanzapine in the rat: effects on body weight, inflammatory, metabolic and microbiota parameters. Psychopharmacology (Berl). 2012;221(1):155-169.
39. Hannestad J, DellaGioia N, Bloch M. The effect of antidepressant medication treatment on serum levels of inflammatory cytokines: a meta-analysis. Neuropsychopharmacology. 2011;36(12):2452-2459.
40. Heijtz RD, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108:3047-3052.
41. Neufeld KAM, Perez-Burgos A, Mao YK, et al. The gut microbiome restores intrinsic and extrinsic nerve function in germfree mice accompanied by changes in calbindin. Neurogastroenterol Motil. 2015;27(5):627-636.
42. Braniste V, Al-Asmakh M, Kowal C, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263):263ra158.
43. Neufeld KM, Kang N, Bienenstock J, et al. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil. 2011;23(3):255-264.
44. Gareau MG, Wine E, Rodrigues DM, et al. Bacterial infection causes stress-induced memory dysfunction in mice. Gut. 2011;60(3):307-317.
45. Bercik P, Denou E, Collins J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141(2):599-609.e3.
46. Bercik P, Park AJ, Sinclair D, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011;23(12):1132-1139.
47. Bravo JA, Forsythe P, Chew MV, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108(38):16050-16055.
48. Hamer HM, De Preter V, Windey K, et al. Functional analysis of colonic bacterial metabolism: relevant to health? Am J Physiol Gastrointest Liver Physiol. 2012;302:G1-G9.
49. Fukumoto S, Tatewaki M, Yamada T, et al. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am J Physiol Regul Integr Comp Physiol. 2003;284(5):R1269-R1276.
50. Hamer HM, Jonkers D, Venema K, et al. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008;27(2):104-119.
51. Yano JM, Yu K, Donaldson GP, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell. 2015;161(2):264-276.
52. Schroeder FA, Lin CL, Crusio WE, et al. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry. 2007;62(1):55-64.
53. Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 2012;56:184-196.
54. Hughes R, Kurth MJ, McGilligan V, et al. Effect of colonic bacterial metabolites on Caco-2 cell paracellular permeability in vitro. Nutr Cancer. 2008;60:259-266.
55. McCall IC, Betanzos A, Weber DA, et al. Effects of phenol on barrier function of a human intestinal epithelial cell line correlate with altered tight junction protein localization. Toxicol Appl Pharmacol. 2009;241:61-70.
56. Lyte M. Microbial endocrinology in the microbiome-gut-brain axis: how bacterial production and utilization of neurochemicals influence behavior. PLoS Pathog. 2013;9(11):e1003726.
57. Al-Nedawi K, Mian MF, Hossain N, et al. Gut commensal microvesicles reproduce parent bacterial signals to host immune and enteric nervous systems. FASEB J. 2015;29(2):684-695.
58. Shen Y, Torchia MLG, Lawson GW, et al. Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe. 2012;12(4):509-520.
59. Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A. 2009;106:3698-3703.
60. Desbonnet L, Garrett L, Clarke G, et al. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res. 2008;43(2):164-174.
61. Perez-Burgos A, Mao Y-K, Bienenstock J, et al. The gut-brain axis rewired: adding a functional vagal nicotinic "sensory synapse." FASEB J. 2014;28(7):3064-3074.
62. Goodnick PJ, Rush AJ, George MS, et al. Vagus nerve stimulation in depression. Expert Opin Pharmacother. 2001;2(7):1061-1063.
63. Cristancho P, Cristancho MA, Baltuch GH, et al. Effectiveness and safety of vagus nerve stimulation for severe treatment-resistant major depression in clinical practice after FDA approval: outcomes at 1 year. J Clin Psychiatry. 2011;72(10):1376-1382.
64. García-Navarrete E, Torres CV, Gallego I, et al. Long-term results of vagal nerve stimulation for adults with medication-resistant epilepsy who have been on unchanged antiepileptic medication. Seizure. 2013;22(1):9-13.
65. Sudo N, Chida Y, Aiba Y, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558(pt 1):263-275.
66. Leclercq S, Matamoros S, Cani PD, et al. Intestinal permeability, gut-bacterial dysbiosis, and behavioral markers of alcohol-dependence severity. Proc Natl Acad Sci U S A. 2014;111(42): E4485-E4493.
67. Jiang H, Ling Z, Zhang Y, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186-194.
68. Naseribafrouei A, Hestad K, Avershina E, et al. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil. 2014;26(8):1155-1162.
69. Szczesniak O, Hestad K, Hanssen JF, et al. Isovaleric acid in stool correlates with human depression. Nutr Neurosci. 2015Feb 24; Epub ahead of print.
70. Bailey MT, Dowd SE, Galley JD, et al. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2011;25(3):397-407.
71. DiGiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PloS One. 2008;3(8):e3056.
72. Jiménez E, Fernández L, Marín ML, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005;51(4):270-274.
73. Jiménez E, Marín ML, Martín R, et al. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008;159(3):187-193.
74. Aagaard K, Ma J, Antony KM, et al. The placenta harbors a unique microbiome. Sci Transl Med. 2014;6(237):237ra65.
75. Funkhouser LJ, Bordenstein SR. Mom knows best: the Universality of Maternal Microbial Transmission. PLoS Biol. 2013;11(8):e1001631.
76. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108(suppl 1):4554-4561.
77. Modi SR, Collins JJ, Relman DA. Antibiotics and the gut microbiota. J Clin Invest. 2014;124(10):4212-4218.
78. Matamoros S, Gras-Leguen C, Le Vacon F, et al. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol. 2013;21(4):167-173.
79. Palmer C, Bik EM, DiGiulio DB, et al. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5(7):e177.
80. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222-227.
81. Bäckhed F, Roswall J, Peng Y, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690-703.
82. Bailey MT, Lubach GR, Coe CL. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr. 2004;38(4):414-421.
83. O'Mahony SM, Marchesi JR, Scully P, et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry. 2009;65(3):263-267.
84. Sánchez MM, Ladd CO, Plotsky PM. Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol. 2001;13(3):419-449.
85. Gareau MG, Jury J, MacQueen G, et al. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut. 2007;56(11):1522-1528.
86. Barreau F, Ferrier L, Fioramonti J, et al. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut. 2004;53(4):501-506.
87. Neufeld KA, Kang N, Bienenstock J, et al. Effects of intestinal microbiota on anxiety-like behavior. Commun Integr Biol. 2011;4(4):492-494.
88. Desbonnet L, Clarke G, et al. Microbiota is essential for social development in the mouse. Mol Psychiatry. 2014;19(2):146-148.
89. McDade TW, Borja JB, Adair LS, et al. Depressive symptoms are not associated with inflammation in younger and older adults in the Philippines. Evol Med Public Health. 2013;2013(1):18-23.
90. McDade TW. Early environments and the ecology of inflammation. Proc Natl Acad Sci U S A. 2012;109(Suppl 2):17281-17288.
91. Rook GAW, Raison CL, Lowry CA. Microbiota, immunoregulatory old friends and psychiatric disorders. Adv Exp Med Biol. 2014;817:319-356.
92. Bailer J, Witthöft M, Wagner H, et al. Childhood maltreatment is associated with depression but not with hypochondriasis in later life. J Psychosom Res. 2014;77(2):104-108.
93. Bernet CZ, Stein MB. Relationship of childhood maltreatment to the onset and course of major depression in adulthood. Depress Anxiety. 1999;9(4):169-174.
94. Gibb BE, Chelminski I, Zimmerman M. Childhood emotional, physical, and sexual abuse, and diagnoses of depressive and anxiety disorders in adult psychiatric outpatients. Depress Anxiety. 2007;24(4):256-263.
95. Cattaneo A, Macchi F, Plazzotta G, et al. Inflammation and neuronal plasticity: a link between childhood trauma and depression pathogenesis. Front Cell Neurosci. 2015;9(40):1-12.
96. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci. 2004;7(8):841-846.
97. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol. 1999;35(2):146-155.
98. Zijlmans MAC, Korpela K, Riksen-Walraven JM, et al. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology. 2015;53:233-245.
99. Kozyrskyj AL, Ernst P, Becker AB. Increased risk of childhood asthma from antibiotic use in early life. Chest. 2007;131(6):1753-1759.
100. Stensballe LG, Simonsen J, Jensen SM, et al. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr. 2013;162(4):832-838.e3.
101. Bailey LC, Forrest CB, Zhang P, et al. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 2014;168(11):1063-1069.
102. Murphy R, Stewart AW, Braithwaite I, et al. Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes (Lond). 2014;38(8):1115-1119.
103. Cox LM, Yamanishi S, Sohn J, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158(4):705-721.
104. Russell SL, Gold MJ, Hartmann M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 2012;13(5):440-447.
105. Benton D, Williams C, Brown A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur J Clin Nutr. 2006;61(3):355-361.
106. Rao AV, Bested AC, Beaulne TM, et al. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009;1(1):6.
107. Messaoudi M, Lalonde R, Violle N, et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr. 2011;105(05):755-764.
108. Messaoudi M, Violle N, Bisson J-F, et al. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes. 2011;2(4):256-261.
109. Tillisch K, Labus J, Kilpatrick L, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology. 2013;144(7):1394-1401.
110. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science. 2010;330(6012):1768-1773.
111. Olszak T, An D, Zeissig S, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336(6080):489-493.