1932

Abstract

The traditional fields of pharmacology and toxicology are beginning to consider the substantial impact our gut microbiota has on host physiology. The microbiota-gut-brain axis is emerging as a particular area of interest and a potential new therapeutic target for effective treatment of central nervous system disorders, in addition to being a potential cause of drug side effects. Microbiota-gut-brain axis signaling can occur via several pathways, including via the immune system, recruitment of host neurochemical signaling, direct enteric nervous system routes and the vagus nerve, and the production of bacterial metabolites. Altered gut microbial profiles have been described in several psychiatric and neurological disorders. Psychobiotics, live biotherapeutics or substances whose beneficial effects on the brain are bacterially mediated, are currently being investigated as direct and/or adjunctive therapies for psychiatric and neurodevelopmental disorders and possibly for neurodegenerative disease, and they may emerge as new therapeutic options in the clinical management of brain disorders.

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2020-01-06
2024-05-24
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Literature Cited

  1. 1. 
    Sender R, Fuchs S, Milo R 2016. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–40
    [Google Scholar]
  2. 2. 
    Hum. Microbiome Proj. Consort 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207–14
    [Google Scholar]
  3. 3. 
    Shkoporov AN, Hill C. 2019. Bacteriophages of the human gut: the “known unknown” of the microbiome. Cell Host Microbe 25:195–209
    [Google Scholar]
  4. 4. 
    Forbes JD, Bernstein CN, Tremlett H, Van Domselaar G, Knox NC 2018. A fungal world: Could the gut mycobiome be involved in neurological disease?. Front. Microbiol. 9:3249
    [Google Scholar]
  5. 5. 
    Konturek SJ, Konturek JW, Pawlik T, Brzozowski T 2004. Brain-gut axis and its role in the control of food intake. J. Physiol. Pharmacol. 55:137–54
    [Google Scholar]
  6. 6. 
    Dinan TG, Cryan JF, Stanton C 2018. Gut microbes and brain development have black box connectivity. Biol. Psychiatry 83:97–99
    [Google Scholar]
  7. 7. 
    Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G et al. 2010. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. PNAS 107:11971–75
    [Google Scholar]
  8. 8. 
    Ng PC. 2000. The fetal and neonatal hypothalamic-pituitary-adrenal axis. Arch. Dis. Child Fetal Neonatal Ed. 82:F250–54
    [Google Scholar]
  9. 9. 
    Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ et al. 2014. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11:506–14
    [Google Scholar]
  10. 10. 
    Tamburini S, Shen N, Wu HC, Clemente JC 2016. The microbiome in early life: implications for health outcomes. Nat. Med. 22:713–22
    [Google Scholar]
  11. 11. 
    Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG et al. 2015. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int. J. Obes. 39:665–70
    [Google Scholar]
  12. 12. 
    Metsala J, Lundqvist A, Virta LJ, Kaila M, Gissler M, Virtanen SM 2015. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin. Exp. Allergy 45:137–45
    [Google Scholar]
  13. 13. 
    Vatanen T, Plichta DR, Somani J, Munch PC, Arthur TD et al. 2019. Genomic variation and strain-specific functional adaptation in the human gut microbiome during early life. Nat. Microbiol. 4:470–79
    [Google Scholar]
  14. 14. 
    Sandhu KV, Sherwin E, Schellekens H, Stanton C, Dinan TG, Cryan JF 2017. Feeding the microbiota-gut-brain axis: diet, microbiome, and neuropsychiatry. Transl. Res. 179:223–44
    [Google Scholar]
  15. 15. 
    De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB et al. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. PNAS 107:14691–96
    [Google Scholar]
  16. 16. 
    McFadzean R. 2014. Exercise can help modulate human gut microbiota PhD Thesis, Univ. Colorado Boulder, CO:
  17. 17. 
    Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M et al. 2014. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63:1913–20
    [Google Scholar]
  18. 18. 
    O'Sullivan O, Cronin O, Clarke SF, Murphy EF, Molloy MG et al. 2015. Exercise and the microbiota. Gut Microbes 6:131–36
    [Google Scholar]
  19. 19. 
    Antunes LC, Han J, Ferreira RB, Lolic P, Borchers CH, Finlay BB 2011. Effect of antibiotic treatment on the intestinal metabolome. Antimicrob. Agents Chemother. 55:1494–503
    [Google Scholar]
  20. 20. 
    Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y et al. 2016. Population-level analysis of gut microbiome variation. Science 352:560–64
    [Google Scholar]
  21. 21. 
    Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M et al. 2016. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352:565–69
    [Google Scholar]
  22. 22. 
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–63
    [Google Scholar]
  23. 23. 
    Mitsou EK, Kakali A, Antonopoulou S, Mountzouris KC, Yannakoulia M et al. 2017. Adherence to the Mediterranean diet is associated with the gut microbiota pattern and gastrointestinal characteristics in an adult population. Br. J. Nutr. 117:1645–55
    [Google Scholar]
  24. 24. 
    Sonnenburg JL, Backhed F. 2016. Diet-microbiota interactions as moderators of human metabolism. Nature 535:56–64
    [Google Scholar]
  25. 25. 
    Sarkar A, Lehto SM, Harty S, Dinan TG, Cryan JF, Burnet PWJ 2016. Psychobiotics and the manipulation of bacteria-gut-brain signals. Trends Neurosci 39:763–81
    [Google Scholar]
  26. 26. 
    Kennedy PJ, Cryan JF, Dinan TG, Clarke G 2017. Kynurenine pathway metabolism and the microbiota-gut-brain axis. Neuropharmacology 112:399–412
    [Google Scholar]
  27. 27. 
    Clarke G, Stilling RM, Kennedy PJ, Stanton C, Cryan JF, Dinan TG 2014. Minireview: gut microbiota: the neglected endocrine organ. Mol. Endocrinol. 28:1221–38
    [Google Scholar]
  28. 28. 
    Rea K, Dinan TG, Cryan JF 2016. The microbiome: a key regulator of stress and neuroinflammation. Neurobiol. Stress 4:23–33
    [Google Scholar]
  29. 29. 
    Vanuytsel T, van Wanrooy S, Vanheel H, Vanormelingen C, Verschueren S et al. 2014. Psychological stress and corticotropin-releasing hormone increase intestinal permeability in humans by a mast cell–dependent mechanism. Gut 63:1293–99
    [Google Scholar]
  30. 30. 
    Alonso C, Guilarte M, Vicario M, Ramos L, Rezzi S et al. 2012. Acute experimental stress evokes a differential gender-determined increase in human intestinal macromolecular permeability. Neurogastroenterol. Motil. 24:740–46
    [Google Scholar]
  31. 31. 
    Fulling C, Dinan TG, Cryan JF 2019. Gut microbe to brain signaling: what happens in vagus…. Neuroview 101:998–1002
    [Google Scholar]
  32. 32. 
    Svensson E, Horvath-Puho E, Thomsen RW, Djurhuus JC, Pedersen L et al. 2015. Vagotomy and subsequent risk of Parkinson's disease. Ann. Neurol. 78:522–29
    [Google Scholar]
  33. 33. 
    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM et al. 2011. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. PNAS 108:16050–55
    [Google Scholar]
  34. 34. 
    Breit S, Kupferberg A, Rogler G, Hasler G 2018. Vagus nerve as modulator of the brain-gut axis in psychiatric and inflammatory disorders. Front. Psychiatry 9:44
    [Google Scholar]
  35. 35. 
    Daban C, Martinez-Aran A, Cruz N, Vieta E 2008. Safety and efficacy of vagus nerve stimulation in treatment-resistant depression: a systematic review. J. Affect. Disord. 110:1–15
    [Google Scholar]
  36. 36. 
    Cristancho P, Cristancho MA, Baltuch GH, Thase ME, O'Reardon JP 2011. 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 72:1376–82
    [Google Scholar]
  37. 37. 
    Han W, Tellez LA, Perkins MH, Perez IO, Qu T et al. 2018. A neural circuit for gut-induced reward. Cell 175:665–78.e23
    [Google Scholar]
  38. 38. 
    Kaelberer MM, Buchanan KL, Klein ME, Barth BB, Montoya MM et al. 2018. A gut-brain neural circuit for nutrient sensory transduction. Science 361:eaat5236
    [Google Scholar]
  39. 39. 
    Bellono NW, Bayrer JR, Leitch DB, Castro J, Zhang C et al. 2017. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170:185–98.e16
    [Google Scholar]
  40. 40. 
    Kelly JR, Borre Y, O'Brien C, Patterson E, El Aidy S et al. 2016. Transferring the blues: Depression-associated gut microbiota induces neurobehavioural changes in the rat. J. Psychiatr. Res. 82:109–18
    [Google Scholar]
  41. 41. 
    Allen AP, Dinan TG, Clarke G, Cryan JF 2017. A psychology of the human brain-gut-microbiome axis. Soc. Personal. Psychol. Compass 11:e12309
    [Google Scholar]
  42. 42. 
    Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J, Forsythe P 2016. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology 63:217–27
    [Google Scholar]
  43. 43. 
    Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH 2007. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56:1522–28
    [Google Scholar]
  44. 44. 
    Golubeva AV, Crampton S, Desbonnet L, Edge D, O'Sullivan O et al. 2015. Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood. Psychoneuroendocrinology 60:58–74
    [Google Scholar]
  45. 45. 
    O'Mahony SM, Hyland NP, Dinan TG, Cryan JF 2011. Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology 214:71–88
    [Google Scholar]
  46. 46. 
    Partrick KA, Chassaing B, Beach LQ, McCann KE, Gewirtz AT, Huhman KL 2018. Acute and repeated exposure to social stress reduces gut microbiota diversity in Syrian hamsters. Behav. Brain Res. 345:39–48
    [Google Scholar]
  47. 47. 
    Bailey MT, Coe CL. 1999. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev. Psychobiol. 35:146–55
    [Google Scholar]
  48. 48. 
    Bailey MT, Lubach GR, Coe CL 2004. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J. Pediatr. Gastroenterol. Nutr. 38:414–21
    [Google Scholar]
  49. 49. 
    Foster JA, Rinaman L, Cryan JF 2017. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol. Stress 7:124–36
    [Google Scholar]
  50. 50. 
    Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N et al. 2004. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 558:263–75
    [Google Scholar]
  51. 51. 
    Clarke G, Grenham S, Scully P, Fitzgerald P, Moloney RD et al. 2013. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry 18:666–73
    [Google Scholar]
  52. 52. 
    Kennedy PJ, Cryan JF, Dinan TG, Clarke G 2014. Irritable bowel syndrome: a microbiome-gut-brain axis disorder?. World J. Gastroenterol. 20:14105–25
    [Google Scholar]
  53. 53. 
    Labus JS, Hollister EB, Jacobs J, Kirbach K, Oezguen N et al. 2017. Differences in gut microbial composition correlate with regional brain volumes in irritable bowel syndrome. Microbiome 5:49
    [Google Scholar]
  54. 54. 
    Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C 2015. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53:233–45
    [Google Scholar]
  55. 55. 
    Naseribafrouei A, Hestad K, Avershina E, Sekelja M, Linlokken A et al. 2014. Correlation between the human fecal microbiota and depression. Neurogastroenterol. Motil. 26:1155–62
    [Google Scholar]
  56. 56. 
    Zheng P, Zeng B, Zhou C, Liu M, Fang Z et al. 2016. Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism. Mol. Psychiatry 21:786–96
    [Google Scholar]
  57. 57. 
    Aizawa E, Tsuji H, Asahara T, Takahashi T, Teraishi T et al. 2016. Possible association of Bifidobacterium and Lactobacillus in the gut microbiota of patients with major depressive disorder. J. Affect. Disord. 202:254–57
    [Google Scholar]
  58. 58. 
    Jiang H, Ling Z, Zhang Y, Mao H, Ma Z et al. 2015. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 48:186–94
    [Google Scholar]
  59. 59. 
    Huang Y, Shi X, Li Z, Shen Y, Shi X et al. 2018. Possible association of Firmicutes in the gut microbiota of patients with major depressive disorder. Neuropsychiatr. Dis. Treat. 14:3329–37
    [Google Scholar]
  60. 60. 
    Valles-Colomer M, Falony G, Darzi Y, Tigchelaar EF, Wang J et al. 2019. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat. Microbiol. 4:623–32
    [Google Scholar]
  61. 61. 
    Dinan TG, Cryan JF. 2019. Gut microbes and depression: still waiting for Godot. Brain Behav. Immun. 79:1–2
    [Google Scholar]
  62. 62. 
    Unger MM, Spiegel J, Dillmann KU, Grundmann D, Philippeit H et al. 2016. Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls. Parkinsonism Relat. Disord. 32:66–72
    [Google Scholar]
  63. 63. 
    Bedarf JR, Hildebrand F, Coelho LP, Sunagawa S, Bahram M et al. 2017. Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson's disease patients. Genome Med 9:39
    [Google Scholar]
  64. 64. 
    Hasegawa S, Goto S, Tsuji H, Okuno T, Asahara T et al. 2015. Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson's disease. PLOS ONE 10:e0142164
    [Google Scholar]
  65. 65. 
    Hill-Burns EM, Debelius JW, Morton JT, Wissemann WT, Lewis MR et al. 2017. Parkinson's disease and Parkinson's disease medications have distinct signatures of the gut microbiome. Mov. Disord. 32:739–49
    [Google Scholar]
  66. 66. 
    Keshavarzian A, Green SJ, Engen PA, Voigt RM, Naqib A et al. 2015. Colonic bacterial composition in Parkinson's disease. Mov. Disord. 30:1351–60
    [Google Scholar]
  67. 67. 
    Scheperjans F, Aho V, Pereira PA, Koskinen K, Paulin L et al. 2015. Gut microbiota are related to Parkinson's disease and clinical phenotype. Mov. Disord. 30:350–58
    [Google Scholar]
  68. 68. 
    Sampson TR, Debelius JW, Thron T, Janssen S, Shastri GG et al. 2016. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell 167:1469–80.e12
    [Google Scholar]
  69. 69. 
    Braak H, de Vos RA, Bohl J, Del Tredici K 2006. Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci. Lett. 396:67–72
    [Google Scholar]
  70. 70. 
    Liu B, Fang F, Pedersen NL, Tillander A, Ludvigsson JF et al. 2017. Vagotomy and Parkinson disease: a Swedish register–based matched-cohort study. Neurology 88:1996–2002
    [Google Scholar]
  71. 71. 
    Dobbs SM, Dobbs RJ, Weller C, Charlett A, Bjarnason IT et al. 2010. Differential effect of Helicobacter pylori eradication on time-trends in brady/hypokinesia and rigidity in idiopathic parkinsonism. Helicobacter 15:279–94
    [Google Scholar]
  72. 72. 
    Shen X, Yang H, Wu Y, Zhang D, Jiang H 2017. Meta-analysis: association of Helicobacter pylori infection with Parkinson's diseases. Helicobacter 22:e12398
    [Google Scholar]
  73. 73. 
    Dardiotis E, Tsouris Z, Mentis AA, Siokas V, Michalopoulou A et al. 2018. H. pylori and Parkinson's disease: meta-analyses including clinical severity. Clin. Neurol. Neurosurg. 175:16–24
    [Google Scholar]
  74. 74. 
    Vogt NM, Kerby RL, Dill-McFarland KA, Harding SJ, Merluzzi AP et al. 2017. Gut microbiome alterations in Alzheimer's disease. Sci. Rep. 7:13537
    [Google Scholar]
  75. 75. 
    Zhuang ZQ, Shen LL, Li WW, Fu X, Zeng F et al. 2018. Gut microbiota is altered in patients with Alzheimer's disease. J. Alzheimers Dis. 63:1337–46
    [Google Scholar]
  76. 76. 
    Arnold SE, Arvanitakis Z, Macauley-Rambach SL, Koenig AM, Wang HY et al. 2018. Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums. Nat. Rev. Neurol. 14:168–81
    [Google Scholar]
  77. 77. 
    Nho K, Kueider-Paisley A, MahmoudianDehkordi S, Arnold M, Risacher SL et al. 2019. Altered bile acid profile in mild cognitive impairment and Alzheimer's disease: relationship to neuroimaging and CSF biomarkers. Alzheimers Dement 15:232–44
    [Google Scholar]
  78. 78. 
    Manderino L, Carroll I, Azcarate-Peril MA, Rochette A, Heinberg L et al. 2017. Preliminary evidence for an association between the composition of the gut microbiome and cognitive function in neurologically healthy older adults. J. Int. Neuropsychol. Soc. 23:700–5
    [Google Scholar]
  79. 79. 
    Cattaneo A, Cattane N, Galluzzi S, Provasi S, Lopizzo N et al. 2017. Association of brain amyloidosis with pro-inflammatory gut bacterial taxa and peripheral inflammation markers in cognitively impaired elderly. Neurobiol. Aging 49:60–68
    [Google Scholar]
  80. 80. 
    Severance EG, Prandovszky E, Castiglione J, Yolken RH 2015. Gastroenterology issues in schizophrenia: why the gut matters. Curr. Psychiatry Rep. 17:27
    [Google Scholar]
  81. 81. 
    Severance EG, Gressitt KL, Stallings CR, Katsafanas E, Schweinfurth LA et al. 2017. Probiotic normalization of Candida albicans in schizophrenia: a randomized, placebo-controlled, longitudinal pilot study. Brain Behav. Immun. 62:41–45
    [Google Scholar]
  82. 82. 
    Zheng P, Zeng B, Liu M, Chen J, Pan J et al. 2019. The gut microbiome from patients with schizophrenia modulates the glutamate-glutamine-GABA cycle and schizophrenia-relevant behaviors in mice. Sci. Adv. 5: eaau8317
    [Google Scholar]
  83. 83. 
    Coury DL, Ashwood P, Fasano A, Fuchs G, Geraghty M et al. 2012. Gastrointestinal conditions in children with autism spectrum disorder: developing a research agenda. Pediatrics 130: Suppl. 2 S160–68
    [Google Scholar]
  84. 84. 
    Strati F, Cavalieri D, Albanese D, De Felice C, Donati C et al. 2017. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 5:24
    [Google Scholar]
  85. 85. 
    Mayer EA, Padua D, Tillisch K 2014. Altered brain-gut axis in autism: comorbidity or causative mechanisms?. Bioessays 36:933–39
    [Google Scholar]
  86. 86. 
    Coretti L, Paparo L, Riccio MP, Amato F, Cuomo M et al. 2018. Gut microbiota features in young children with autism spectrum disorders. Front. Microbiol. 9:3146
    [Google Scholar]
  87. 87. 
    Sandler RH, Finegold SM, Bolte ER, Buchanan CP, Maxwell AP et al. 2000. Short-term benefit from oral vancomycin treatment of regressive-onset autism. J. Child Neurol. 15:429–35
    [Google Scholar]
  88. 88. 
    Kang DW, Adams JB, Gregory AC, Borody T, Chittick L et al. 2017. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5:10
    [Google Scholar]
  89. 89. 
    Aizawa E, Tsuji H, Asahara T, Takahashi T, Teraishi T et al. 2018. Bifidobacterium and Lactobacillus counts in the gut microbiota of patients with bipolar disorder and healthy controls. Front. Psychiatry 9:730
    [Google Scholar]
  90. 90. 
    Hemmings SMJ, Malan-Muller S, van den Heuvel LL, Demmitt BA, Stanislawski MA et al. 2017. The microbiome in posttraumatic stress disorder and trauma-exposed controls: an exploratory study. Psychosom. Med. 79:936–46
    [Google Scholar]
  91. 91. 
    Dinan TG, Stanton C, Cryan JF 2013. Psychobiotics: a novel class of psychotropic. Biol. Psychiatry 74:720–26
    [Google Scholar]
  92. 92. 
    Cussotto S, Clarke G, Dinan TG, Cryan JF 2019. Psychotropics and the microbiome: a chamber of secrets. Psychopharmacology 236:1411–32
    [Google Scholar]
  93. 93. 
    Butler MI, Sandhu K, Cryan JF, Dinan TG 2019. From isoniazid to psychobiotics: the gut microbiome as a new antidepressant target. Br. J. Hosp. Med. 80:139–45
    [Google Scholar]
  94. 94. 
    Kelly JR, Allen AP, Temko A, Hutch W, Kennedy PJ et al. 2017. Lost in translation? The potential psychobiotic Lactobacillus rhamnosus (JB-1) fails to modulate stress or cognitive performance in healthy male subjects. Brain Behav. Immun. 61:50–59
    [Google Scholar]
  95. 95. 
    Ng QX, Peters C, Ho CYX, Lim DY, Yeo WS 2018. A meta-analysis of the use of probiotics to alleviate depressive symptoms. J. Affect. Disord. 228:13–19
    [Google Scholar]
  96. 96. 
    Ostlund-Lagerstrom L, Kihlgren A, Repsilber D, Bjorksten B, Brummer RJ, Schoultz I 2016. Probiotic administration among free-living older adults: a double blinded, randomized, placebo-controlled clinical trial. Nutr. J. 15:80
    [Google Scholar]
  97. 97. 
    Bambury A, Sandhu K, Cryan JF, Dinan TG 2018. Finding the needle in the haystack: systematic identification of psychobiotics. Br. J. Pharmacol. 175:4430–38
    [Google Scholar]
  98. 98. 
    O'Toole PW, Marchesi JR, Hill C 2017. Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat. Microbiol. 2:17057
    [Google Scholar]
  99. 99. 
    Benton D, Williams C, Brown A 2007. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur. J. Clin. Nutr. 61:355–61
    [Google Scholar]
  100. 100. 
    Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H et al. 2016. Clinical and metabolic response to probiotic administration in patients with major depressive disorder: a randomized, double-blind, placebo-controlled trial. Nutrition 32:315–20
    [Google Scholar]
  101. 101. 
    Kazemi A, Noorbala AA, Azam K, Eskandari MH, Djafarian K 2018. Effect of probiotic and prebiotic versus placebo on psychological outcomes in patients with major depressive disorder: a randomized clinical trial. Clin. Nutr. 38:522–28
    [Google Scholar]
  102. 102. 
    Pinto-Sanchez MI, Hall GB, Ghajar K, Nardelli A, Bolino C et al. 2017. Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology 153:448–59.e8
    [Google Scholar]
  103. 103. 
    Messaoudi M, Violle N, Bisson JF, Desor D, Javelot H, Rougeot C 2011. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2:256–61
    [Google Scholar]
  104. 104. 
    Diop L, Guillou S, Durand H 2008. Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: a double-blind, placebo-controlled, randomized trial. Nutr. Res. 28:1–5
    [Google Scholar]
  105. 105. 
    Colica C, Avolio E, Bollero P, Costa de Miranda R, Ferraro S et al. 2017. Evidences of a new psychobiotic formulation on body composition and anxiety. Mediators Inflamm 2017:5650627
    [Google Scholar]
  106. 106. 
    Steenbergen L, Sellaro R, van Hemert S, Bosch JA, Colzato LS 2015. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 48:258–64
    [Google Scholar]
  107. 107. 
    Slykerman RF, Hood F, Wickens K, Thompson JMD, Barthow C et al. 2017. Effect of Lactobacillus rhamnosus HN001 in pregnancy on postpartum symptoms of depression and anxiety: a randomised double-blind placebo-controlled trial. EBioMedicine 24:159–65
    [Google Scholar]
  108. 108. 
    Allen AP, Hutch W, Borre YE, Kennedy PJ, Temko A et al. 2016. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl. Psychiatry 6:e939
    [Google Scholar]
  109. 109. 
    Takada M, Nishida K, Kataoka-Kato A, Gondo Y, Ishikawa H et al. 2016. Probiotic Lactobacillus casei strain Shirota relieves stress-associated symptoms by modulating the gut-brain interaction in human and animal models. Neurogastroenterol. Motil. 28:1027–36
    [Google Scholar]
  110. 110. 
    Rao AV, Bested AC, Beaulne TM, Katzman MA, Iorio C et al. 2009. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog 1:6
    [Google Scholar]
  111. 111. 
    Andersson H, Tullberg C, Ahrne S, Hamberg K, Lazou Ahren I et al. 2016. Oral administration of Lactobacillus plantarum 299v reduces cortisol levels in human saliva during examination induced stress: a randomized, double-blind controlled trial. Int. J. Microbiol. 2016:8469018
    [Google Scholar]
  112. 112. 
    Mohammadi AA, Jazayeri S, Khosravi-Darani K, Solati Z, Mohammadpour N et al. 2016. The effects of probiotics on mental health and hypothalamic-pituitary-adrenal axis: a randomized, double-blind, placebo-controlled trial in petrochemical workers. Nutr. Neurosci. 19:387–95
    [Google Scholar]
  113. 113. 
    Nishihira J, Kagami-Katsuyama H, Tanaka A, Nishimura M, Kobayashi T, Kawasaki Y 2014. Elevation of natural killer cell activity and alleviation of mental stress by the consumption of yogurt containing Lactobacillus gasseri SBT2055 and Bifidobacterium longum SBT2928 in a double-blind, placebo-controlled clinical trial. J. Funct. Foods 11:261–68
    [Google Scholar]
  114. 114. 
    Chong HX, Yusoff NAA, Hor YY, Lew LC, Jaafar MH et al. 2019. Lactobacillus plantarum DR7 alleviates stress and anxiety in adults: a randomised, double-blind, placebo-controlled study. Benef. Microbes 10:355–73
    [Google Scholar]
  115. 115. 
    Miyaoka T, Kanayama M, Wake R, Hashioka S, Hayashida M et al. 2018. Clostridium butyricum MIYAIRI 588 as adjunctive therapy for treatment-resistant major depressive disorder: a prospective open-label trial. Clin. Neuropharmacol. 41:151–55
    [Google Scholar]
  116. 116. 
    Wallace CJK, Milev R. 2017. The effects of probiotics on depressive symptoms in humans: a systematic review. Ann. Gen. Psychiatry 16:14
    [Google Scholar]
  117. 117. 
    Pirbaglou M, Katz J, de Souza RJ, Stearns JC, Motamed M, Ritvo P 2016. Probiotic supplementation can positively affect anxiety and depressive symptoms: a systematic review of randomized controlled trials. Nutr. Res. 36:889–98
    [Google Scholar]
  118. 118. 
    Huang R, Wang K, Hu J 2016. Effect of probiotics on depression: a systematic review and meta-analysis of randomized controlled trials. Nutrients 8:483
    [Google Scholar]
  119. 119. 
    Chung YC, Jin HM, Cui Y, Kim DS, Jung JM et al. 2014. Fermented milk of Lactobacillus helveticus IDCC3801 improves cognitive functioning during cognitive fatigue tests in healthy older adults. J. Funct. Foods 10:465–74
    [Google Scholar]
  120. 120. 
    Romijn AR, Rucklidge JJ, Kuijer RG, Frampton C 2017. A double-blind, randomized, placebo-controlled trial of Lactobacillus helveticus and Bifidobacterium longum for the symptoms of depression. Aust. N. Z. J. Psychiatry 51:810–21
    [Google Scholar]
  121. 121. 
    Akbari E, Asemi Z, Daneshvar Kakhaki R, Bahmani F, Kouchaki E et al. 2016. Effect of probiotic supplementation on cognitive function and metabolic status in Alzheimer's disease: a randomized, double-blind and controlled trial. Front. Aging Neurosci. 8:256
    [Google Scholar]
  122. 122. 
    Agahi A, Hamidi GA, Daneshvar R, Hamdieh M, Soheili M et al. 2018. Does severity of Alzheimer's disease contribute to its responsiveness to modifying gut microbiota? A double blind clinical trial. Front. Neurol. 9:662
    [Google Scholar]
  123. 123. 
    Rudzki L, Ostrowska L, Pawlak D, Malus A, Pawlak K et al. 2018. Probiotic Lactobacillus plantarum 299v decreases kynurenine concentration and improves cognitive functions in patients with major depression: a double-blind, randomized, placebo controlled study. Psychoneuroendocrinology 100:213–22
    [Google Scholar]
  124. 124. 
    Ceccarelli G, Brenchley JM, Cavallari EN, Scheri GC, Fratino M et al. 2017. Impact of high-dose multi-strain probiotic supplementation on neurocognitive performance and central nervous system immune activation of HIV-1 infected individuals. Nutrients 9:1269
    [Google Scholar]
  125. 125. 
    Bagga D, Reichert JL, Koschutnig K, Aigner CS, Holzer P et al. 2018. Probiotics drive gut microbiome triggering emotional brain signatures. Gut Microbes 9:486–96
    [Google Scholar]
  126. 126. 
    Wang X, Yang J, Zhang H, Yu J, Yao Z 2019. Oral probiotic administration during pregnancy prevents autism-related behaviors in offspring induced by maternal immune activation via anti-inflammation in mice. Autism Res 12:576–88
    [Google Scholar]
  127. 127. 
    El-Ansary A, Bacha AB, Bjorklund G, Al-Orf N, Bhat RS et al. 2018. Probiotic treatment reduces the autistic-like excitation/inhibition imbalance in juvenile hamsters induced by orally administered propionic acid and clindamycin. Metab. Brain Dis. 33:1155–64
    [Google Scholar]
  128. 128. 
    Patusco R, Ziegler J. 2018. Role of probiotics in managing gastrointestinal dysfunction in children with autism spectrum disorder: an update for practitioners. Adv. Nutr. 9:637–50
    [Google Scholar]
  129. 129. 
    Shaaban SY, El Gendy YG, Mehanna NS, El-Senousy WM, El-Feki HSA et al. 2018. The role of probiotics in children with autism spectrum disorder: a prospective, open-label study. Nutr. Neurosci. 21:676–81
    [Google Scholar]
  130. 130. 
    Dickerson FB, Stallings C, Origoni A, Katsafanas E, Savage CL et al. 2014. Effect of probiotic supplementation on schizophrenia symptoms and association with gastrointestinal functioning: a randomized, placebo-controlled trial. Prim. Care Companion CNS Disord. 16: PCC.13m01579
    [Google Scholar]
  131. 131. 
    Tomasik J, Yolken RH, Bahn S, Dickerson FB 2015. Immunomodulatory effects of probiotic supplementation in schizophrenia patients: a randomized, placebo-controlled trial. Biomark Insights 10:47–54
    [Google Scholar]
  132. 132. 
    Okubo R, Koga M, Katsumata N, Odamaki T, Matsuyama S et al. 2019. Effect of Bifidobacterium breve A-1 on anxiety and depressive symptoms in schizophrenia: a proof-of-concept study. J. Affect. Disord. 245:377–85
    [Google Scholar]
  133. 133. 
    Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA et al. 2017. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat. Rev. Gastroenterol. Hepatol. 14:491–502
    [Google Scholar]
  134. 134. 
    Verkhnyatskaya S, Ferrari M, de Vos P, Walvoort MTC 2019. Shaping the infant microbiome with non-digestible carbohydrates. Front. Microbiol. 10:343
    [Google Scholar]
  135. 135. 
    Schmidt K, Cowen PJ, Harmer CJ, Tzortzis G, Errington S, Burnet PW 2015. Prebiotic intake reduces the waking cortisol response and alters emotional bias in healthy volunteers. Psychopharmacology 232:1793–801
    [Google Scholar]
  136. 136. 
    Silk DB, Davis A, Vulevic J, Tzortzis G, Gibson GR 2009. Clinical trial: the effects of a trans-galactooligosaccharide prebiotic on faecal microbiota and symptoms in irritable bowel syndrome. Aliment Pharmacol. Ther. 29:508–18
    [Google Scholar]
  137. 137. 
    Grimaldi R, Gibson GR, Vulevic J, Giallourou N, Castro-Mejia JL et al. 2018. A prebiotic intervention study in children with autism spectrum disorders (ASDs). Microbiome 6:133
    [Google Scholar]
  138. 138. 
    Flowers SA, Baxter NT, Ward KM, Kraal AZ, McInnis MG et al. 2019. Effects of atypical antipsychotic treatment and resistant starch supplementation on gut microbiome composition in a cohort of patients with bipolar disorder or schizophrenia. Pharmacotherapy 39:161–70
    [Google Scholar]
  139. 139. 
    Barichella M, Pacchetti C, Bolliri C, Cassani E, Iorio L et al. 2016. Probiotics and prebiotic fiber for constipation associated with Parkinson disease: an RCT. Neurology 87:1274–80
    [Google Scholar]
  140. 140. 
    Gocan AG, Bachg D, Schindler AE, Rohr UD 2012. Balancing steroidal hormone cascade in treatment-resistant veteran soldiers with PTSD using a fermented soy product (FSWW08): a pilot study. Horm. Mol. Biol. Clin. Investig. 10:301–14
    [Google Scholar]
  141. 141. 
    Sanctuary MR, Kain JN, Chen SY, Kalanetra K, Lemay DG et al. 2019. Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms. PLOS ONE 14:e0210064
    [Google Scholar]
  142. 142. 
    Sanna S, van Zuydam NR, Mahajan A, Kurilshikov A, Vich Vila A et al. 2019. Causal relationships among the gut microbiome, short-chain fatty acids and metabolic diseases. Nat. Genet. 51:600–5
    [Google Scholar]
  143. 143. 
    van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C et al. 2018. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations. J. Physiol. 596:4923–44
    [Google Scholar]
  144. 144. 
    Shultz SR, MacFabe DF, Ossenkopp KP, Scratch S, Whelan J et al. 2008. Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 54:901–11
    [Google Scholar]
  145. 145. 
    Lach G, Schellekens H, Dinan TG, Cryan JF 2018. Anxiety, depression, and the microbiome: a role for gut peptides. Neurotherapeutics 15:36–59
    [Google Scholar]
  146. 146. 
    de Almada CN, Almada CN, Martinez RCR, Sant'Ana AS 2016. Paraprobiotics: evidences on their ability to modify biological responses, inactivation methods and perspectives on their application in foods. Trends Food Sci. Technol. 58:96–114
    [Google Scholar]
  147. 147. 
    Nishida K, Sawada D, Kuwano Y, Tanaka H, Sugawara T et al. 2017. Daily administration of paraprobiotic Lactobacillus gasseri CP2305 ameliorates chronic stress-associated symptoms in Japanese medical students. J. Funct. Foods 36:112–21
    [Google Scholar]
  148. 148. 
    Wei CL, Wang S, Yen JT, Cheng YF, Liao CL et al. 2019. Antidepressant-like activities of live and heat-killed Lactobacillus paracasei PS23 in chronic corticosterone-treated mice and possible mechanisms. Brain Res 1711:202–13
    [Google Scholar]
  149. 149. 
    Liu WH, Chuang HL, Huang YT, Wu CC, Chou GT et al. 2016. Alteration of behavior and monoamine levels attributable to Lactobacillus plantarum PS128 in germ-free mice. Behav. Brain Res. 298:202–9
    [Google Scholar]
  150. 150. 
    Aslam H, Green J, Jacka FN, Collier F, Berk M et al. 2018. Fermented foods, the gut and mental health: a mechanistic overview with implications for depression and anxiety. Nutr. Neurosci. In press. https://doi.org/10.1080/1028415X.2018.1544332
    [Crossref] [Google Scholar]
  151. 151. 
    Tillisch K, Labus J, Kilpatrick L, Jiang Z, Stains J et al. 2013. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology 144:1394–401.e4
    [Google Scholar]
  152. 152. 
    Kato-Kataoka A, Nishida K, Takada M, Suda K, Kawai M et al. 2016. Fermented milk containing Lactobacillus casei strain Shirota prevents the onset of physical symptoms in medical students under academic examination stress. Benef. Microbes 7:153–56
    [Google Scholar]
  153. 153. 
    Simren M, Ohman L, Olsson J, Svensson U, Ohlson K et al. 2010. Clinical trial: the effects of a fermented milk containing three probiotic bacteria in patients with irritable bowel syndrome—a randomized, double-blind, controlled study. Aliment Pharmacol. Ther. 31:218–27
    [Google Scholar]
  154. 154. 
    Lassale C, Batty GD, Baghdadli A, Jacka F, Sanchez-Villegas A et al. 2018. Healthy dietary indices and risk of depressive outcomes: a systematic review and meta-analysis of observational studies. Mol. Psychiatry 24:965–86
    [Google Scholar]
  155. 155. 
    Jacka FN, Pasco JA, Mykletun A, Williams LJ, Hodge AM et al. 2010. Association of Western and traditional diets with depression and anxiety in women. Am. J. Psychiatry 167:305–11
    [Google Scholar]
  156. 156. 
    Psaltopoulou T, Sergentanis TN, Panagiotakos DB, Sergentanis IN, Kosti R, Scarmeas N 2013. Mediterranean diet, stroke, cognitive impairment, and depression: a meta-analysis. Ann. Neurol. 74:580–91
    [Google Scholar]
  157. 157. 
    Li Y, Lv MR, Wei YJ, Sun L, Zhang JX et al. 2017. Dietary patterns and depression risk: a meta-analysis. Psychiatry Res 253:373–82
    [Google Scholar]
  158. 158. 
    Molendijk M, Molero P, Sanchez-Pedreno FO, Van der Does W, Martinez-Gonzalez MA 2018. Diet quality and depression risk: a systematic review and dose-response meta-analysis of prospective studies. J. Affect. Disord. 226:346–54
    [Google Scholar]
  159. 159. 
    Shafiei F, Salari-Moghaddam A, Larijani B, Esmaillzadeh A 2019. Adherence to the Mediterranean diet and risk of depression: a systematic review and updated meta-analysis of observational studies. Nutr. Rev. 77:230–39
    [Google Scholar]
  160. 160. 
    Jacka FN, O'Neil A, Opie R, Itsiopoulos C, Cotton S et al. 2017. A randomised controlled trial of dietary improvement for adults with major depression (the ‘SMILES’ trial). BMC Med 15:23
    [Google Scholar]
  161. 161. 
    Chatterton ML, Mihalopoulos C, O'Neil A, Itsiopoulos C, Opie R et al. 2018. Economic evaluation of a dietary intervention for adults with major depression (the “SMILES” trial). BMC Public Health 18:599
    [Google Scholar]
  162. 162. 
    Forsyth A, Deane FP, Williams P 2015. A lifestyle intervention for primary care patients with depression and anxiety: a randomised controlled trial. Psychiatry Res 230:537–44
    [Google Scholar]
  163. 163. 
    Parletta N, Zarnowiecki D, Cho J, Wilson A, Bogomolova S et al. 2019. A Mediterranean-style dietary intervention supplemented with fish oil improves diet quality and mental health in people with depression: a randomized controlled trial (HELFIMED). Nutr. Neurosci. 22:474–87
    [Google Scholar]
  164. 164. 
    Firth J, Marx W, Dash S, Carney R, Teasdale SB et al. 2019. The effects of dietary improvement on symptoms of depression and anxiety: a meta-analysis of randomized controlled trials. Psychosom. Med. 81:265–80
    [Google Scholar]
  165. 165. 
    Morkl S, Wagner-Skacel J, Lahousen T, Lackner S, Holasek SJ et al. 2018. The role of nutrition and the gut-brain axis in psychiatry: a review of the literature. Neuropsychobiology In press. https://doi.org/10.1159/000492834
    [Crossref] [Google Scholar]
  166. 166. 
    Forslund K, Hildebrand F, Nielsen T, Falony G, Le Chatelier E et al. 2015. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528:262–66
    [Google Scholar]
  167. 167. 
    Imhann F, Bonder MJ, Vich Vila A, Fu J, Mujagic Z et al. 2016. Proton pump inhibitors affect the gut microbiome. Gut 65:740–48
    [Google Scholar]
  168. 168. 
    Freedberg DE, Toussaint NC, Chen SP, Ratner AJ, Whittier S et al. 2015. Proton pump inhibitors alter specific taxa in the human gastrointestinal microbiome: a crossover trial. Gastroenterology 149:883–85.e9
    [Google Scholar]
  169. 169. 
    Jackson MA, Goodrich JK, Maxan ME, Freedberg DE, Abrams JA et al. 2016. Proton pump inhibitors alter the composition of the gut microbiota. Gut 65:749–56
    [Google Scholar]
  170. 170. 
    Takagi T, Naito Y, Inoue R, Kashiwagi S, Uchiyama K et al. 2018. The influence of long-term use of proton pump inhibitors on the gut microbiota: an age-sex-matched case-control study. J. Clin. Biochem. Nutr. 62:100–5
    [Google Scholar]
  171. 171. 
    Maier L, Pruteanu M, Kuhn M, Zeller G, Telzerow A et al. 2018. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555:623–28
    [Google Scholar]
  172. 172. 
    Cussotto S, Strain CR, Fouhy F, Strain RG, Peterson VL et al. 2018. Differential effects of psychotropic drugs on microbiome composition and gastrointestinal function. Psychopharmacology 236:1671–85
    [Google Scholar]
  173. 173. 
    Dinan TG, Cryan JF. 2018. Schizophrenia and the microbiome: time to focus on the impact of antipsychotic treatment on the gut microbiota. World J. Biol. Psychiatry 19:568–70
    [Google Scholar]
  174. 174. 
    Davey KJ, Cotter PD, O'Sullivan O, Crispie F, Dinan TG et al. 2013. Antipsychotics and the gut microbiome: olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat. Transl. Psychiatry 3:e309
    [Google Scholar]
  175. 175. 
    Davey KJ, O'Mahony SM, Schellekens H, O'Sullivan O, Bienenstock J et al. 2012. Gender-dependent consequences of chronic olanzapine in the rat: effects on body weight, inflammatory, metabolic and microbiota parameters. Psychopharmacology 221:155–69
    [Google Scholar]
  176. 176. 
    Lyte M, Daniels KM, Schmitz-Esser S 2019. Fluoxetine-induced alteration of murine gut microbial community structure: evidence for a microbial endocrinology-based mechanism of action responsible for fluoxetine-induced side effects. PeerJ 7:e6199
    [Google Scholar]
  177. 177. 
    Liskiewicz P, Pelka-Wysiecka J, Kaczmarczyk M, Loniewski I, Wronski M et al. 2019. Fecal microbiota analysis in patients going through a depressive episode during treatment in a psychiatric hospital setting. J. Clin. Med. 8:164
    [Google Scholar]
  178. 178. 
    van Kessel SP, Frye AK, El-Gendy AO, Castejon M, Keshavarzian A et al. 2019. Gut bacterial tyrosine decarboxylases restrict levels of levodopa in the treatment of Parkinson's disease. Nat. Commun. 10:310
    [Google Scholar]
  179. 179. 
    Kao AC, Spitzer S, Anthony DC, Lennox B, Burnet PWJ 2018. Prebiotic attenuation of olanzapine-induced weight gain in rats: analysis of central and peripheral biomarkers and gut microbiota. Transl. Psychiatry 8:66
    [Google Scholar]
  180. 180. 
    Kumar H, Salminen S, Verhagen H, Rowland I, Heimbach J et al. 2015. Novel probiotics and prebiotics: road to the market. Curr. Opin. Biotechnol. 32:99–103
    [Google Scholar]
  181. 181. 
    Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J et al. 2010. Safety assessment of probiotics for human use. Gut Microbes 1:164–85
    [Google Scholar]
  182. 182. 
    Herman L, Chemaly M, Cocconcelli PS, Fernandez P, Klein G et al. 2019. The qualified presumption of safety assessment and its role in EFSA risk evaluations: 15 years past. FEMS Microbiol. Lett. 366: fny260
    [Google Scholar]
  183. 183. 
    Cryan JF, Clarke G, Dinan TG, Schellekens H 2018. A microbial drugstore for motility. Cell Host Microbe 23:691–92
    [Google Scholar]
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