Is there a dysbiosis in individuals with a neurodevelopmental disorder compared to controls over the course of development? A systematic review

Dall’Aglio L, Muka T, Cecil CAM, Bramer WM, Verbiest MMPJ, Nano J et al (2018) The role of epigenetic modifications in neurodevelopmental disorders: a systematic review. Neurosci Biobehav Rev 94:17–30 Keil KP, Lein PJ (2016) DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? Environ Epigenet 2(1):dvv012 Thapar A, Cooper M, Eyre O, Langley K (2013) Practitioner review: what have we learnt about the causes of ADHD? J Child Psychol Psychiatry 54:3–16 Tordjman S, Somogyi E, Coulon N, Kermarrec S, Cohen D, Bronsard G et al (2014) Gene × environment interactions in autism spectrum disorders: role of epigenetic mechanisms. Front Psychiatry 5:53 Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM (2017) Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med 23:314–326 Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N 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 107:11971–11975 Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A et al (2016) Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med 22:250–253 Bastiaanssen TFS, Cowan CSM, Claesson MJ, Dinan TG, Cryan JF (2019) Making Sense of … the microbiome in psychiatry. Int J Neuropsychopharmacol 22:37–52 Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H et al (2016) Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med 8:343ra82 David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563 Wu GD, Chen J, Hoffmann C, Bittinger K, Chen Y-Y, Keilbaugh SA et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science (New York, N.y). 334:105–108 De Filippis F, Pellegrini N, Vannini L, Jeffery IB, La Storia A, Laghi L et al (2016) High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome. Gut 65:1812–1821 Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M (2011) Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced Immunomodulation. Brain Behav Immun 25:397–407 Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35:146–155 O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho A-M, Quigley EMM et al (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiat 65:263–267 O’Mahony SM, Hyland NP, Dinan TG, Cryan JF (2011) Maternal separation as a model of brain–gut axis dysfunction. Psychopharmacology 214:71–88 Cong X, Henderson WA, Graf J, McGrath JM (2015) Early life experience and gut microbiome: the brain-gut-microbiota signaling system. Adv Neonatal Care 15:314–323 Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C et al (2010) A human gut microbial gene catalog established by metagenomic sequencing. Nature 464:59–65 Claesson MJ, Clooney AG, O’Toole PW (2017) A clinician’s guide to microbiome analysis. Nat Rev Gastroenterol Hepatol 14:585–595 Foster JA, McVey Neufeld K-A (2013) Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci 36:305–312 Fond G, Chevalier G, Eberl G, Leboyer M (2016) Le rôle potentiel du microbiote intestinal dans les troubles psychiatriques majeurs : mécanismes, données fondamentales, comorbidités gastro-intestinales et options thérapeutiques. La Presse Médicale 45:7–19 Cryan JF, Dinan TG (2015) More than a gut feeling: the microbiota regulates neurodevelopment and behavior. Neuropsychopharmacology 40:241–242 Hoban AE, Stilling RM, Ryan FJ, Shanahan F, Dinan TG, Claesson MJ et al (2016) Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry 6:e774 Luczynski P, Whelan SO, O’Sullivan C, Clarke G, Shanahan F, Dinan TG et al (2016) Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus. Eur J Neurosci 44:2654–2666 Dinan TG, Cryan JF (2017) Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol 595:489–503 Neufeld K-AM, Kang N, Bienenstock J, Foster JA (2011) Effects of intestinal microbiota on anxiety-like behavior. Commun Integr Biol 4:492–494 Kang D-W, Adams JB, Gregory AC, Borody T, Chittick L, Fasano A et al (2017) Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome 5:10 Ma Y, Chen H, Lan C, Ren J (2018) Help, hope and hype: ethical considerations of human microbiome research and applications. Protein Cell 9:404–415 Adams JB, Johansen LJ, Powell LD, Quig D, Rubin RA. Gastrointestinal flora and gastrointestinal status in children with autism – comparisons to typical children and correlation with autism severity. BMC Gastroenterology [Internet]. 2011 [cited 2019 Jan 4];11. https://bmcgastroenterol.biomedcentral.com/articles/10.1186/1471-230X-11-22. Accessed 4 Jan 2019 Williams BL, Hornig M, Buie T, Bauman ML, Cho Paik M, Wick I et al (2011) Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. Jacobson S, editor. PLoS ONE 6:24e585 Williams BL, Hornig M, Parekh T, Lipkin WI. Application of Novel PCR-Based Methods for Detection, Quantitation, and Phylogenetic Characterization of Sutterella Species in Intestinal Biopsy Samples from Children with Autism and Gastrointestinal Disturbances. mBio [Internet]. 2012 [cited 2019 Jan 4];3. Available from: https://mbio.asm.org/cgi/doi/10.1128/mBio.00261-11. Accessed 4 Jan 2019 Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA (2012) Elevated fecal short chain fatty acid and ammonia concentrations in children with autism spectrum disorder. Dig Dis Sci 57:2096–2102 Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA (2011) Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl Environ Microbiol 77:6718–6721 Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA (2013) Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder. Mol Autism 4:42 Tomova A, Husarova V, Lakatosova S, Bakos J, Vlkova B, Babinska K et al (2015) Gastrointestinal microbiota in children with autism in Slovakia. Physiol Behav 138:179–187 Strati F, Cavalieri D, Albanese D, De Felice C, Donati C, Hayek J, et al. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome [Internet]. 2017 [cited 2019 Jan 4];5. Available from: https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-017-0242-1. Accessed 4 Jan 2019 Son JS, Zheng LJ, Rowehl LM, Tian X, Zhang Y, Zhu W et al (2015) Comparison of fecal microbiota in children with autism spectrum disorders and neurotypical siblings in the simons simplex collection. Heimesaat MM, editor. PLoS ONE 10:e0137725 Rose DR, Yang H, Serena G, Sturgeon C, Ma B, Careaga M et al (2018) Differential immune responses and microbiota profiles in children with autism spectrum disorders and co-morbid gastrointestinal symptoms. Brain Behav Immun 70:354–368 Qiao Y, Wu M, Feng Y, Zhou Z, Chen L, Chen F (2018) Alterations of oral microbiota distinguish children with autism spectrum disorders from healthy controls. Scientific Reports [Internet]. 2018 [cited 2019 Jan 4];8. https://www.nature.com/articles/s41598-018-19982-y. Accessed 4 Jan 2019 Pusponegoro HD, Ismael S, Sastroasmoro S, Firmansyah A, Vandenplas Y (2015) Maladaptive behavior and gastrointestinal disorders in children with autism spectrum disorder. Pediatric Gastroenterol Hepatol Nutr 18:230 Pulikkan J, Maji A, Dhakan DB, Saxena R, Mohan B, Anto MM et al (2018) Gut Microbial dysbiosis in indian children with autism spectrum disorders. Microb Ecol 76:1102–1114 Parracho HM, Bingham MO, Gibson GR, McCartney AL (2005) Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. J Med Microbiol 54:987–991 Martirosian G, Ekiel A, Aptekorz M, Wiechuła B, Kazek B, Jankowska-Steifer E et al (2011) Fecal lactoferrin and Clostridium spp. in stools of autistic children. Anaerobe 17:43–45 Lee Y, Park J-Y, Lee E-H, Yang J, Jeong B-R, Kim Y-K et al (2017) Rapid assessment of microbiota changes in individuals with autism spectrum disorder using bacteria-derived membrane vesicles in urine. Exp Neurobiol 26:307 Kushak RI, Winter HS, Buie TM, Cox SB, Phillips CD, Ward NL (2017) Analysis of the duodenal microbiome in autistic individuals: association with carbohydrate digestion. J Pediatr Gastroenterol Nutr 64:e110–e116 Kantarcioglu AS, Kiraz N, Aydin A (2016) Microbiota–gut–brain axis: yeast species isolated from stool samples of children with suspected or diagnosed autism spectrum disorders and in vitro susceptibility against nystatin and fluconazole. Mycopathologia 181:1–7 Kang D-W, Park JG, Ilhan ZE, Wallstrom G, LaBaer J, Adams JB et al (2013) Reduced incidence of prevotella and other fermenters in intestinal microflora of autistic children. Gilbert JA, editor. PLoS ONE 8:68322 Kang D-W, Ilhan ZE, Isern NG, Hoyt DW, Howsmon DP, Shaffer M et al (2018) Differences in fecal microbial metabolites and microbiota of children with autism spectrum disorders. Anaerobe 49:121–131 Iovene MR, Bombace F, Maresca R, Sapone A, Iardino P, Picardi A et al (2017) Intestinal dysbiosis and yeast isolation in stool of subjects with autism spectrum disorders. Mycopathologia 182:349–363 Góra B, Gofron Z, Grosiak M, Aptekorz M, Kazek B, Kocelak P et al (2018) Toxin profile of fecal Clostridium perfringens strains isolated from children with autism spectrum disorders. Anaerobe 51:73–77 Gondalia SV, Palombo EA, Knowles SR, Cox SB, Meyer D, Austin DW (2012) Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings: GI microbiota of children with autism. Autism Res 5:419–427 Finegold SM, Summanen PH, Downes J, Corbett K, Komoriya T (2017) Detection of Clostridium perfringens toxin genes in the gut microbiota of autistic children. Anaerobe 45:133–137 Finegold SM, Molitoris D, Song Y, Liu C, Vaisanen M, Bolte E et al (2002) Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 35:S6–16 Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD et al (2010) Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 16:444–453 Luna RA, Oezguen N, Balderas M, Venkatachalam A, Runge JK, Versalovic J et al (2017) Distinct microbiome-neuroimmune signatures correlate with functional abdominal pain in children with autism spectrum disorder. Cell Mol Gastroenterol Hepatol 3:218–230 Aarts E, Ederveen THA, Naaijen J, Zwiers MP, Boekhorst J, Timmerman HM et al (2017) Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS ONE 12:e0183509 Jiang H, Zhou Y, Zhou G, Li Y, Yuan J, Li X et al (2018) Gut microbiota profiles in treatment-naïve children with attention deficit hyperactivity disorder. Behav Brain Res 347:408–413 Prehn-Kristensen A, Zimmermann A, Tittmann L, Lieb W, Schreiber S, Baving L et al (2018) Reduced microbiome alpha diversity in young patients with ADHD. Yao Y-G, editor. PLoS ONE 13:e000728 De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A, Serrazzanetti DI et al (2013) Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. Heimesaat MM, editor. PLoS ONE 8:e76993 American Psychiatric Association, editor (2013) Diagnostic and statistical manual of mental disorders: DSM-5. 5. edn. American Psychiatric Publishing, Washington, DC Cenit MC, Nuevo IC, Codoñer-Franch P, Dinan TG, Sanz Y (2017) Gut microbiota and attention deficit hyperactivity disorder: new perspectives for a challenging condition. Eur Child Adolesc Psychiatry 26:1081–1092 Rutayisire E, Huang K, Liu Y, Tao F (2016) The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterology [Internet]. 2016 [cited 2019 Apr 18];16. https://bmcgastroenterol.biomedcentral.com/articles/10.1186/s12876-016-0498-0. Accessed 18 Apr 2019 Goedert JJ (2013) The microbiota and human health: beyond exploration. Eur J Clin Invest 43:657–659 Herpertz-Dahlmann B, Seitz J, Baines J (2017) Food matters: how the microbiome and gut-brain interaction might impact the development and course of anorexia nervosa. Eur Child Adolesc Psychiatry 26:1031–1041 Karlsson F, Tremaroli V, Nielsen J, Bäckhed F (2013) Assessing the human gut microbiota in metabolic diseases. Diabetes 62:3341–3349 Berding K, Donovan SM (2016) Microbiome and nutrition in autism spectrum disorder: current knowledge and research needs. Nutr Rev 74:723–736 Bandini LG, Anderson SE, Curtin C, Cermak S, Evans EW, Scampini R et al (2010) Food selectivity in children with autism spectrum disorders and typically developing children. J Pediatr 157:259–264 DuPont AW, DuPont HL (2011) The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastroenterol Hepatol 8:523–531 Hiergeist A, Reischl U, Gessner A (2016) Multicenter quality assessment of 16S ribosomal DNA-sequencing for microbiome analyses reveals high inter-center variability. Int J Med Microbiol 306:334–342 Fouhy F, Deane J, Rea MC, O’Sullivan Ó, Ross RP, O’Callaghan G et al (2015) The effects of freezing on faecal microbiota as determined using miseq sequencing and culture-based investigations. Neu J, editor. PLoS ONE 10:e0119355 Rintala A, Pietilä S, Munukka E, Eerola E, Pursiheimo JP, Laiho A, Pekkala S, Huovinen P (2017) Gut microbiota analysis results are highly dependent on the 16S rRNA gene target region, whereas the impact of DNA extraction is minor. JBT 28(1):19–30 Hill CJ, Brown JRM, Lynch DB, Jeffery IB, Ryan CA, Ross RP, et al (2016) Effect of room temperature transport vials on DNA quality and phylogenetic composition of faecal microbiota of elderly adults and infants. Microbiome [Internet]. 2016 [cited 2019 Apr 18];4. https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-016-0164-3. Accessed 18 Apr 2019 Panek M, Čipčić Paljetak H, Barešić A, Perić M, Matijašić M, Lojkić I, et al (2018) Methodology challenges in studying human gut microbiota – effects of collection, storage, DNA extraction and next generation sequencing technologies. Scientific Reports [Internet]. 2018 [cited 2019 Apr 18];8. https://www.nature.com/articles/s41598-018-23296-4. Accessed 18 Apr 2019 Guo Y, Li S-H, Kuang Y-S, He J-R, Lu J-H, Luo B-J, et al (2016) Effect of short-term room temperature storage on the microbial community in infant fecal samples. Scientific Reports [Internet]. 2016 [cited 2019 Apr 18];6. https://www.nature.com/articles/srep26648. Accessed 18 Apr 2019 Flores R, Shi J, Yu G, Ma B, Ravel J, Goedert JJ, et al (2015) Collection media and delayed freezing effects on microbial composition of human stool. Microbiome [Internet]. 2015 [cited 2019 Apr 18];3. https://microbiomejournal.biomedcentral.com/articles/10.1186/s40168-015-0092-7. Accessed 18 Apr 2019 Clooney AG, Fouhy F, Sleator RD, O’ Driscoll A, Stanton C, Cotter PD, et al (2016) Comparing apples and oranges? next generation sequencing and its impact on microbiome analysis. PLoS One 11(2):e0148028 Kennedy NA, Walker AW, Berry SH, Duncan SH, Farquarson FM, Louis P et al (2014) The impact of different dna extraction kits and laboratories upon the assessment of human gut microbiota composition by 16S rRNA gene sequencing. Sanz Y, editor. PLoS ONE 9:88982 Fraher MH, O’Toole PW, Quigley EMM (2012) Techniques used to characterize the gut microbiota: a guide for the clinician. Nat Rev Gastroenterol Hepatol 9:312–322 O’Doherty KC, Virani A, Wilcox ES (2016) The human microbiome and public health: social and ethical considerations. Am J Public Health 106:414–420