Advertisement

European Child & Adolescent Psychiatry

, Volume 26, Issue 9, pp 1081–1092 | Cite as

Gut microbiota and attention deficit hyperactivity disorder: new perspectives for a challenging condition

  • María Carmen CenitEmail author
  • Isabel Campillo Nuevo
  • Pilar Codoñer-Franch
  • Timothy G. Dinan
  • Yolanda SanzEmail author
Review

Abstract

A bidirectional communication between the gut and the brain (gut–brain axis) is well recognized with the gut microbiota viewed as a key regulator of this cross-talk. Currently, a body of preclinical and to a lesser extent epidemiological evidence supports the notion that host–microbe interactions play a key role in brain development and function and in the etiology of neurodevelopmental disorders. Early life events and shifts away from traditional lifestyles are known to impact gut microbiota composition and function and, thereby, may increase the risk of developing neurodevelopmental disorders. Attention deficit hyperactivity disorder (ADHD) is nowadays the most prevalent neurodevelopmental disorder. Despite many years of research its etiology is unclear and its diagnosis and treatment are still challenging. Different factors reported to be associated with the risk of developing ADHD and/or linked to different ADHD manifestations have also been linked to shifts in gut microbiota composition, suggesting a link between the microbiota and the disorder. Evidence from preliminary human studies also suggests that dietary components that modulate gut microbiota may also influence ADHD development or symptoms, although further studies are warranted to confirm this hypothesis. Here, we firstly review the potential mechanisms by which the gut microbiota may regulate the brain–gut axis and influence behavior and neurodevelopmental disorders. Secondly, we discuss the current knowledge about the different factors and dietary components reported to be associated with the risk of developing ADHD or its manifestations and with shifts in gut microbiota composition. Finally, we briefly highlight the need to progress our understanding regarding the role of the gut microbiota in ADHD, since this could open new avenues for early intervention and improved management of the disease.

Keywords

Microbiota ADHD Microbiota Gut–brain axis Dysbiosis 

Notes

Acknowledgements

This work was supported by Grant AGL2014-52101-P from the Spanish Ministry of Economy and Competitiveness (MINECO). The Sara Borrell postdoctoral contract of MCC from ISCIII and the PTA contract of IC from MINECO are fully acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. 1.
    Martens G, van Loo K (2007) Genetic and environmental factors in complex neurodevelopmental disorders. Curr Genom 8:429–444CrossRefGoogle Scholar
  2. 2.
    Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry 164:942–948PubMedCrossRefGoogle Scholar
  3. 3.
    Kooij SJJ et al (2010) European consensus statement on diagnosis and treatment of adult ADHD: the European network adult ADHD. BMC Psychiatry 10:67PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Trull TJ, Tragesser SL, Solhan M, Schwartz-Mette R (2007) Dimensional models of personality disorder: diagnostic and statistical manual of mental disorders fifth edition and beyond. Curr Opin Psychiatry 20:52–56PubMedCrossRefGoogle Scholar
  5. 5.
    Larson K, Russ SA, Kahn RS, Halfon N (2011) Patterns of comorbidity, functioning, and service use for US children with ADHD, 2007. Pediatrics 127:462–470PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Dias TGC et al (2013) Developments and challenges in the diagnosis and treatment of ADHD. Rev Bras Psiquiatr 35:S40–S50PubMedCrossRefGoogle Scholar
  7. 7.
    Childress AC, Sallee FR (2014) Attention-deficit/hyperactivity disorder with inadequate response to stimulants: approaches to management. CNS Drugs 28:121–129PubMedCrossRefGoogle Scholar
  8. 8.
    Shyu Y-C et al (2015) Attention-deficit/hyperactivity disorder, methylphenidate use and the risk of developing schizophrenia spectrum disorders: a nationwide population-based study in Taiwan. Schizophr Res 168:161–167PubMedCrossRefGoogle Scholar
  9. 9.
    Martinez-Raga J, Knecht C, Szerman N, Martinez MI (2013) Risk of serious cardiovascular problems with medications for attention-deficit hyperactivity disorder. CNS Drugs 27:15–30PubMedCrossRefGoogle Scholar
  10. 10.
    Sprich S, Biederman J, Crawford MH, Mundy E, Faraone SV (2000) Adoptive and biological families of children and adolescents with ADHD. J Am Acad Child Adolesc Psychiatry 39:1432–1437PubMedCrossRefGoogle Scholar
  11. 11.
    Thapar A, Cooper M, Eyre O, Langley K (2013) Practitioner review: what have we learnt about the causes of ADHD? J Child Psychol Psychiatry 54:3–16PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Sharma A, Couture J (2014) A review of the pathophysiology, etiology, and treatment of attention-deficit hyperactivity disorder (ADHD). Ann Pharmacother 48:209–225PubMedCrossRefGoogle Scholar
  13. 13.
    Banaschewski T, Becker K, Scherag S, Franke B, Coghill D (2010) Molecular genetics of attention-deficit/hyperactivity disorder: an overview. Eur Child Adolesc Psychiatry 19:237–257PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Dinan TG, Cryan JF (2015) The impact of gut microbiota on brain and behaviour: implications for psychiatry. Curr Opin Clin Nutr Metab Care 18:552–558PubMedCrossRefGoogle Scholar
  15. 15.
    Borre YE et al (2014) Microbiota and neurodevelopmental windows: implications for brain disorders. Trends Mol Med. doi: 10.1016/j.molmed.2014.05.002 PubMedGoogle Scholar
  16. 16.
    Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712PubMedCrossRefGoogle Scholar
  17. 17.
    McVey Neufeld K-A, Luczynski P, Seira Oriach C, Dinan TG, Cryan JF (2016) What’s bugging your teen?-The microbiota and adolescent mental health. Neurosci Biobehav Rev. doi: 10.1016/j.neubiorev.2016.06.005 PubMedGoogle Scholar
  18. 18.
    Luczynski P et al (2016) Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior. Int J Neuropsychopharmacol. 19(8). doi: 10.1093/ijnp/pyw020
  19. 19.
    Cryan JF, Dinan TG (2015) More than a gut feeling: the microbiota regulates neurodevelopment and behavior. Neuropsychopharmacology 40:241–242PubMedCrossRefGoogle Scholar
  20. 20.
    De Palma G et al (2015) Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun 6:7735PubMedCrossRefGoogle Scholar
  21. 21.
    Collins SM, Kassam Z, Bercik P (2013) The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Curr Opin Microbiol 16:240–245PubMedCrossRefGoogle Scholar
  22. 22.
    Rogers GB et al (2016) From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways. Mol Psychiatry 21:738–748PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Lyte M (2011) Probiotics function mechanistically as delivery vehicles for neuroactive compounds: microbial endocrinology in the design and use of probiotics. Bioessays 33:574–581PubMedCrossRefGoogle Scholar
  24. 24.
    Bercik P et al (2011) The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 141:599–609 (609.e1–3) PubMedCrossRefGoogle Scholar
  25. 25.
    Collins SM, Bercik P (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136:2003–2014PubMedCrossRefGoogle Scholar
  26. 26.
    Barrett E, Ross RP, O’Toole PW, Fitzgerald GF, Stanton C (2012) γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113:411–417PubMedCrossRefGoogle Scholar
  27. 27.
    Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74:720–726PubMedCrossRefGoogle Scholar
  28. 28.
    Clarke G et al (2012) A distinct profile of tryptophan metabolism along the kynurenine pathway downstream of toll-like receptor activation in irritable bowel syndrome. Front Pharmacol 3:90PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    O’Mahony SM, Clarke G, Borre YE, Dinan TG, Cryan JF (2014) Serotonin, tryptophan metabolism and the brain–gut- microbiome axis. Behav Brain Res 277:32–48PubMedCrossRefGoogle Scholar
  30. 30.
    Maes M, Mihaylova I, Ruyter M De, Kubera M, Bosmans E (2007) The immune effects of TRYCATs (tryptophan catabolites along the IDO pathway): relevance for depression—and other conditions characterized by tryptophan depletion induced by inflammation. Neuro Endocrinol Lett 28:826–831PubMedGoogle Scholar
  31. 31.
    Guillemin GJ (2012) Quinolinic acid, the inescapable neurotoxin. FEBS J 279:1356–1365PubMedCrossRefGoogle Scholar
  32. 32.
    O’ Mahony SM, Clarke G, Dinan TG, Cryan JF (2015) Early life adversity and brain development: is the microbiome a missing piece of the puzzle? Neuroscience. doi: 10.1016/j.neuroscience.2015.09.068
  33. 33.
    Clarke G et al (2013) The microbiome-gut–brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry 18:666–673PubMedCrossRefGoogle Scholar
  34. 34.
    Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG (2008) The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 43:164–174PubMedCrossRefGoogle Scholar
  35. 35.
    Foley KA, MacFabe DF, Vaz A, Ossenkopp K-P, Kavaliers M (2014) Sexually dimorphic effects of prenatal exposure to propionic acid and lipopolysaccharide on social behavior in neonatal, adolescent, and adult rats: implications for autism spectrum disorders. Int J Dev Neurosci 39:68–78PubMedCrossRefGoogle Scholar
  36. 36.
    MacFabe DF et al (2007) Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders. Behav Brain Res 176:149–169PubMedCrossRefGoogle Scholar
  37. 37.
    Stilling RM, Dinan TG, Cryan JF (2014) Microbial genes, brain and behaviour-epigenetic regulation of the gut–brain axis. Genes Brain Behav 13:69–86PubMedCrossRefGoogle Scholar
  38. 38.
    Erny D et al (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18:965–977PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Corominas-Roso M et al (2013) Decreased serum levels of brain-derived neurotrophic factor in adults with attention-deficit hyperactivity disorder. Int J Neuropsychopharmacol 1–9. doi: 10.1017/S1461145712001629
  40. 40.
    Sucksdorff M et al (2015) Preterm birth and poor fetal growth as risk factors of attention-deficit/hyperactivity disorder. Pediatrics. doi: 10.1542/peds.2015-1043 PubMedGoogle Scholar
  41. 41.
    Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246–254PubMedCrossRefGoogle Scholar
  42. 42.
    Zijlmans MAC, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C (2015) Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology 53:233–245PubMedCrossRefGoogle Scholar
  43. 43.
    Barrett E et al (2013) The individual-specific and diverse nature of the preterm infant microbiota. Arch Dis Child Fetal Neonatal Ed 98:F334–F340PubMedCrossRefGoogle Scholar
  44. 44.
    Jakobsson HE et al (2014) Decreased gut microbiota diversity, delayed bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut 63:559–566PubMedCrossRefGoogle Scholar
  45. 45.
    Grönlund MM, Lehtonen OP, Eerola E, Kero P (1999) Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 28:19–25PubMedCrossRefGoogle Scholar
  46. 46.
    Dominguez-Bello MG et al (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA 107:11971–11975PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Boksa P, El-Khodor BF (2003) Birth insult interacts with stress at adulthood to alter dopaminergic function in animal models: possible implications for schizophrenia and other disorders. Neurosci Biobehav Rev 27:91–101PubMedCrossRefGoogle Scholar
  48. 48.
    Curran EA et al (2015) Association between obstetric mode of delivery and autism spectrum disorder: a population-based sibling design study. JAMA psychiatry 72:935–942PubMedCrossRefGoogle Scholar
  49. 49.
    Curran EA et al (2015) Research review: birth by caesarean section and development of autism spectrum disorder and attention-deficit/hyperactivity disorder: a systematic review and meta-analysis. J Child Psychol Psychiatry 56:500–508PubMedCrossRefGoogle Scholar
  50. 50.
    Talge NM, Allswede DM, Holzman C (2016) Gestational age at term, delivery circumstance, and their association with childhood attention deficit hyperactivity disorder symptoms. Paediatr Perinat Epidemiol 30:171–180PubMedCrossRefGoogle Scholar
  51. 51.
    Amiri S, Malek A, Sadegfard M, Abdi S (2012) Pregnancy-related maternal risk factors of attention-deficit hyperactivity disorder: a case-control study. ISRN Pediatr 2012:458064PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Chu S-M et al (2012) The relationship between attention deficit hyperactivity disorder and premature infants in Taiwanese: a case control study. BMC Psychiatry 12:85PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Johnson S et al (2016) Antecedents of attention-deficit/hyperactivity disorder symptoms in children born extremely preterm. J Dev Behav Pediatr 37:285–297PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Becattini S, Taur Y, Pamer EG (2016) Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol Med 22:458–478PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Sternbach H, State R (1997) Antibiotics: neuropsychiatric effects and psychotropic interactions. Harv Rev Psychiatry 5:214–226PubMedCrossRefGoogle Scholar
  56. 56.
    Van den Bergh BRH, Marcoen A (2004) High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 75:1085–1097PubMedCrossRefGoogle Scholar
  57. 57.
    Li J, Olsen J, Vestergaard M, Obel C (2010) Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. Eur Child Adolesc Psychiatry 19:747–753PubMedCrossRefGoogle Scholar
  58. 58.
    Grizenko N, Shayan YR, Polotskaia A, Ter-Stepanian M, Joober R (2008) Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD. J Psychiatry Neurosci 33:10–16PubMedPubMedCentralGoogle Scholar
  59. 59.
    Culhane JF et al (2001) Maternal stress is associated with bacterial vaginosis in human pregnancy. Matern Child Health J 5:127–134PubMedCrossRefGoogle Scholar
  60. 60.
    Sudo N et al (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 558:263–275PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Sterley T-L, Howells FM, Russell VA (2013) Maternal separation increases GABA(A) receptor-mediated modulation of norepinephrine release in the hippocampus of a rat model of ADHD, the spontaneously hypertensive rat. Brain Res 1497:23–31PubMedCrossRefGoogle Scholar
  62. 62.
    Womersley JS, Hsieh JH, Kellaway LA, Gerhardt GA, Russell VA (2011) Maternal separation affects dopamine transporter function in the spontaneously hypertensive rat: an in vivo electrochemical study. Behav Brain Funct 7:49PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Sanz Y (2016) Bifidobacteria in Foods: health Effects. Encycl Food Heal 1:388–394CrossRefGoogle Scholar
  64. 64.
    Mann JR, McDermott S (2011) Are maternal genitourinary infection and pre-eclampsia associated with ADHD in school-aged children? J Atten Disord 15:667–673PubMedCrossRefGoogle Scholar
  65. 65.
    Silva D, Colvin L, Hagemann E, Bower C (2014) Environmental risk factors by gender associated with attention-deficit/hyperactivity disorder. Pediatrics 133:e14–e22PubMedCrossRefGoogle Scholar
  66. 66.
    Hsiao EY et al (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451–1463PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Derecki NC et al (2010) Regulation of learning and memory by meningeal immunity: a key role for IL-4. J Exp Med 207:1067–1080PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Ceylan MF et al (2014) Increased levels of serum neopterin in attention deficit/hyperactivity disorder (ADHD). J Neuroimmunol. doi: 10.1016/j.jneuroim.2014.06.002 PubMedGoogle Scholar
  69. 69.
    Rivera HM, Christiansen KJ, Sullivan EL (2015) The role of maternal obesity in the risk of neuropsychiatric disorders. Front Neurosci 9:194PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Jo H et al (2015) Maternal prepregnancy body mass index and child psychosocial development at 6 years of age. Pediatrics 135:e1198–e1209PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Rodriguez A et al (2008) Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes (Lond) 32:550–557CrossRefGoogle Scholar
  72. 72.
    Kang SS, Kurti A, Fair DA, Fryer JD (2014) Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring. J Neuroinflammation 11:156PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Cabrera-Rubio R et al (2012) The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr 96:544–551PubMedCrossRefGoogle Scholar
  74. 74.
    Cortese S et al (2015) Association between ADHD and obesity: a systematic review and meta-analysis. Am J Psychiatry appiajp201515020266. doi: 10.1176/appi.ajp.2015.15020266
  75. 75.
    Cani PD (2013) Gut microbiota and obesity: lessons from the microbiome. Brief Funct Genom 12:381–387CrossRefGoogle Scholar
  76. 76.
    Foster JA, McVey Neufeld K-A (2013) Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312PubMedCrossRefGoogle Scholar
  77. 77.
    Mimouni-Bloch A et al (2013) Breastfeeding may protect from developing attention-deficit/hyperactivity disorder. Breastfeed Med 8:363–367PubMedCrossRefGoogle Scholar
  78. 78.
    Park S et al (2014) Protective effect of breastfeeding with regard to children’s behavioral and cognitive problems. Nutr J 13:111PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    David LA et al (2013) Diet rapidly and reproducibly alters the human gut microbiome. Nature. doi: 10.1038/nature12820
  80. 80.
    Dash S, Clarke G, Berk M, Jacka FN (2015) The gut microbiome and diet in psychiatry: focus on depression. Curr Opin Psychiatry 28:1–6PubMedCrossRefGoogle Scholar
  81. 81.
    Psaltopoulou T et al (2013) Mediterranean diet, stroke, cognitive impairment, and depression: a meta-analysis. Ann Neurol 74:580–591PubMedCrossRefGoogle Scholar
  82. 82.
    Jacka FN et al (2013) Maternal and early postnatal nutrition and mental health of offspring by age 5 years: a prospective cohort study. J Am Acad Child Adolesc Psychiatry 52:1038–1047PubMedCrossRefGoogle Scholar
  83. 83.
    Konikowska K, Regulska-Ilow B, Rózańska D (2012) The influence of components of diet on the symptoms of ADHD in children. Rocz Państwowego Zakładu Hig 63:127–134Google Scholar
  84. 84.
    Pelsser LM et al (2011) Effects of a restricted elimination diet on the behaviour of children with attention-deficit hyperactivity disorder (INCA study): a randomised controlled trial. Lancet 377:494–503PubMedCrossRefGoogle Scholar
  85. 85.
    Sonuga-Barke EJS et al (2013) Nonpharmacological interventions for ADHD: systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. Am J Psychiatry 170:275–289PubMedCrossRefGoogle Scholar
  86. 86.
    Stulnig TM, Zeyda M (2004) Immunomodulation by polyunsaturated fatty acids: impact on T-cell signaling. Lipids 39:1171–1175PubMedCrossRefGoogle Scholar
  87. 87.
    Kaliannan K, Wang B, Li X-Y, Kim K-J, Kang JX (2015) A host–microbiome interaction mediates the opposing effects of omega-6 and omega-3 fatty acids on metabolic endotoxemia. Sci Rep 5:11276PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Yu H-N et al (2014) Effects of fish oil with a high content of n-3 polyunsaturated fatty acids on mouse gut microbiota. Arch Med Res 45:195–202PubMedCrossRefGoogle Scholar
  89. 89.
    Chassaing B et al (2015) Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519:92–96PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Hawkey E, Nigg JT (2014) Omega-3 fatty acid and ADHD: blood level analysis and meta-analytic extension of supplementation trials. Clin Psychol Rev 34:496–505PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Ferreira CF et al (2014) Correlation between n-3 polyunsaturated fatty acids consumption and BDNF peripheral levels in adolescents. Lipids Health Dis 13:44PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Howard AL et al (2011) ADHD is associated with a ‘Western’ dietary pattern in adolescents. J Atten Disord 15:403–411PubMedCrossRefGoogle Scholar
  93. 93.
    Freeman MP et al (2006) Omega-3 fatty acids: evidence basis for treatment and future research in psychiatry. J Clin Psychiatry 67:1954–1967PubMedCrossRefGoogle Scholar
  94. 94.
    Zhang X-W, Hou W-S, Li M, Tang Z-Y (2015) Omega-3 fatty acids and risk of cognitive decline in the elderly: a meta-analysis of randomized controlled trials. Aging Clin Exp Res. doi: 10.1007/s40520-015-0381-9 Google Scholar
  95. 95.
    Letenneur L, Proust-Lima C, Le Gouge A, Dartigues JF, Barberger-Gateau P (2007) Flavonoid intake and cognitive decline over a 10-year period. Am J Epidemiol 165:1364–1371PubMedCrossRefGoogle Scholar
  96. 96.
    Desideri G et al (2012) Benefits in cognitive function, blood pressure, and insulin resistance through cocoa flavanol consumption in elderly subjects with mild cognitive impairment: the cocoa, cognition, and aging (CoCoA) study. Hypertension 60:794–801PubMedCrossRefGoogle Scholar
  97. 97.
    Dvoráková M et al (2007) Urinary catecholamines in children with attention deficit hyperactivity disorder (ADHD): modulation by a polyphenolic extract from pine bark (pycnogenol). Nutr Neurosci 10:151–157PubMedCrossRefGoogle Scholar
  98. 98.
    Selma MV, Espín JC, Tomás-Barberán FA (2009) Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem 57:6485–6501PubMedCrossRefGoogle Scholar
  99. 99.
    Duda-Chodak A, Tarko T, Satora P, Sroka P (2015) Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review. Eur J Nutr 54:325–341PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Laparra JM, Sanz Y (2010) Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 61:219–225PubMedCrossRefGoogle Scholar
  101. 101.
    McKeown C, Hisle-Gorman E, Eide M, Gorman GH, Nylund CM (2013) Association of constipation and fecal incontinence with attention-deficit/hyperactivity disorder. Pediatrics 132:e1210–e1215PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Stevens LJ, Kuczek T, Burgess JR, Hurt E, Arnold LE (2011) Dietary sensitivities and ADHD symptoms: thirty-five years of research. Clin Pediatr (Phila) 50:279–293CrossRefGoogle Scholar
  103. 103.
    Pärtty A, Kalliomäki M, Wacklin P, Salminen S, Isolauri E (2015) A possible link between early probiotic intervention and the risk of neuropsychiatric disorders later in childhood: a randomized trial. Pediatr Res 77:823–828PubMedCrossRefGoogle Scholar
  104. 104.
    Sekirov I, Russell SL, Antunes LCM, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90:859–904PubMedCrossRefGoogle Scholar
  105. 105.
    Chung H, Kasper DL (2010) Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr Opin Immunol 22:455–460PubMedCrossRefGoogle Scholar
  106. 106.
    Atarashi K, Honda K (2011) Microbiota in autoimmunity and tolerance. Curr Opin Immunol 23:761–768PubMedCrossRefGoogle Scholar
  107. 107.
    Verlaet AAJ, Noriega DB, Hermans N, Savelkoul HFJ (2014) Nutrition, immunological mechanisms and dietary immunomodulation in ADHD. Eur Child Adolesc Psychiatry 23:519–529PubMedCrossRefGoogle Scholar
  108. 108.
    Toral M et al (2014) The probiotic Lactobacillus coryniformis CECT5711 reduces the vascular pro-oxidant and pro-inflammatory status in obese mice. Clin Sci 127:33–45PubMedCrossRefGoogle Scholar
  109. 109.
    Chen L et al (2013) Lactobacillus acidophilus ATCC 4356 attenuates the atherosclerotic progression through modulation of oxidative stress and inflammatory process. Int Immunopharmacol 17:108–115PubMedCrossRefGoogle Scholar
  110. 110.
    Joseph N, Zhang-James Y, Perl A, Faraone SV (2015) Oxidative stress and ADHD: a meta-analysis. J Atten Disord 19:915–924PubMedCrossRefGoogle Scholar
  111. 111.
    Kul M et al (2015) Evaluation of oxidative metabolism in child and adolescent patients with attention deficit hyperactivity disorder. Psychiatry Investig 12:361–366PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Sezen H et al (2016) Increased oxidative stress in children with attention deficit hyperactivity disorder. Redox Rep 21:248–253PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • María Carmen Cenit
    • 1
    • 2
    Email author
  • Isabel Campillo Nuevo
    • 1
  • Pilar Codoñer-Franch
    • 2
    • 3
  • Timothy G. Dinan
    • 4
    • 5
  • Yolanda Sanz
    • 1
    Email author
  1. 1.Microbial Ecology, Nutrition and Health Research Group, Institute of Agrochemistry and Food TechnologyNational Research Council (IATA-CSIC)PaternaSpain
  2. 2.Department of PediatricsDr. Peset University HospitalValenciaSpain
  3. 3.Department of Pediatrics, Obstetrics and GynecologyUniversity of ValenciaValenciaSpain
  4. 4.APC Microbiome InstituteUniversity College CorkCorkIreland
  5. 5.Department of Psychiatry and Neurobehavioural ScienceUniversity College CorkCorkIreland

Personalised recommendations