Gastrointestinal issues in autism spectrum disorder

Harvard Review of Psychiatry

Volumn 22, Issue 2, 2014, Pages 104-111

  Hsiao, Elaine Y ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Gastroenterology; Gut; Immunity; Intestine; Neurodevelopment

Indexed keywords

AUTISM; BRAIN; DISEASE SEVERITY; ENDOPHENOTYPE; GASTROINTESTINAL SYMPTOM; GASTROINTESTINAL TRACT; HUMAN; IMMUNE DYSREGULATION; METABOLIC DISORDER; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COMPLICATION; GASTROINTESTINAL DISEASES; GENETICS;

CHILD DEVELOPMENT DISORDERS, PERVASIVE; ENDOPHENOTYPES; GASTROINTESTINAL DISEASES; HUMANS;

EID: 84902182050     PISSN: 10673229     EISSN: 14657309     Source Type: Journal    
DOI: 10.1097/HRP.0000000000000029     Document Type: Review

References (91)

1. Bauman ML. Medical comorbidities in autism: challenges to diagnosis and treatment. Neurotherapeutics 2010;7:320-7.
2. Kohane IS, McMurry A, Weber G, et al. The co-morbidity burden of children and young adults with autism spectrum disorders. PLoS One 2012;7:e33224.
3. Kanner L. Autistic disturbances of affective contact. Acta Paedopsychiatr 1968;35:100-36.
4. Buie T, Campbell DB, Fuchs GJ 3rd, et al. Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: a consensus report. Pediatrics 2010;125 suppl 1:S1-18.
5. Buie T, Fuchs GJ 3rd, Furuta GT, et al. Recommendations for evaluation and treatment of common gastrointestinal problems in children with ASDs. Pediatrics 2010;125 suppl 1:S19-29.
6. Coury DL, Ashwood P, Fasano A, et al. Gastrointestinal conditions in children with autism spectrum disorder: developing a research agenda. Pediatrics 2012;130 suppl 2:S160-8.
7. D'Eufemia P, Celli M, Finocchiaro R, et al. Abnormal intestinal permeability in children with autism. Acta Paediatr 1996;85: 1076-9. (Pubitemid 26302768)
8. de Magistris L, Familiari V, Pascotto A, et al. Alterations of the intestinal barrier in patients with autism spectrum disorders and in their first-degree relatives. J Pediatr Gastroenterol Nutr 2010;51:418-24.
9. Erickson CA, Stigler KA, Corkins MR, Posey DJ, Fitzgerald JF, McDougle CJ. Gastrointestinal factors in autistic disorder: a critical review. J Autism Dev Disord 2005;35:713-27.
10. Levy SE, Souders MC, Ittenbach RF, Giarelli E, Mulberg AE, Pinto-Martin JA. Relationship of dietary intake to gastrointestinal symptoms in children with autistic spectrum disorders. Biol Psychiatry 2007;61:492-7. (Pubitemid 46185339)
11. Ming X, Stein TP, Barnes V, Rhodes N, Guo L. Metabolic perturbance in autism spectrum disorders: a metabolomics study. J Proteome Res 2012;11:5856-62.
12. Jyonouchi H. Food allergy and autism spectrum disorders: is there a link? Curr Allergy Asthma Rep 2009;9:194-201.
13. Williams BL, Hornig M, Buie T, et al. Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. PLoS One 2011;6:e24585.
14. 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 Gastroenterol 2011;11:22.
15. Finegold SM. State of the art;microbiology in health and disease. Intestinal bacterial flora in autism. Anaerobe 2011;17:367-8.
16. Finegold SM, Dowd SE, Gontcharova V, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010;16:444-53.
17. Gondalia SV, Palombo EA, Knowles SR, Cox SB, Meyer D, Austin DW. Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings. Autism Res 2012;5:419-27.
18. Parracho HM, Bingham MO, Gibson GR, McCartney AL. Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. J Med Microbiol 2005;54:987-91. (Pubitemid 41395858)
19. Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl Environ Microbiol 2011; 77:6718-21.
20. Finegold SM, Molitoris D, Song Y, et al. Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002; 35:S6-16.
21. Song Y, Liu C, Finegold SM. Real-time PCR quantitation of clostridia in feces of autistic children. Appl Environ Microbiol 2004;70:6459-65. (Pubitemid 39518551)
22. 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 2012;3:e00261-11.
23. Heijtz RD, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011;108:3047-52.
24. 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;108:16050-5.
25. Al-Asmakh M, Anuar F, Zadjali F, Rafter J, Pettersson S. Gut microbial communities modulating brain development and function. Gut Microbes 2012;3:366-73.
26. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10:735-42.
27. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 2012;13:701-12.
28. Louis P. Does the human gut microbiota contribute to the etiology of autism spectrum disorders? Dig Dis Sci 2012;57: 1987-9.
29. Persico AM, Napolioni V. Urinary p-cresol in autism spectrum disorder. Neurotoxicol Teratol 2013;36:82-90.
30. Rossignol DA, Frye RE. Mitochondrial dysfunction in autism spectrum disorders: a systematic review and meta-analysis. Mol Psychiatry 2012;17:290-314.
31. Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Elevated fecal short chain fatty acid and ammonia concentrations in children with autism spectrum disorder. Dig Dis Sci 2012;57:2096-102.
32. Yap IK, Angley M, Veselkov KA, Holmes E, Lindon JC, Nicholson JK. Urinary metabolic phenotyping differentiates children with autism from their unaffected siblings and agematched controls. J Proteome Res 2010;9:2996-3004.
33. Black C, Kaye JA, Jick H. Relation of childhood gastrointestinal disorders to autism: nested case-control study using data from the UK General Practice Research Database. BMJ 2002;325:419-21. (Pubitemid 34969792)
34. Horvath K, Papadimitriou JC, Rabsztyn A, Drachenberg C, Tildon JT. Gastrointestinal abnormalities in children with autistic disorder. J Pediatr 1999;135:559-63. (Pubitemid 30180444)
35. Ibrahim SH, Voigt RG, Katusic SK, Weaver AL, Barbaresi WJ. Incidence of gastrointestinal symptoms in children with autism: a population-based study. Pediatrics 2009;124:680-6.
36. Mouridsen SE, Isager T, Rich B. Diseases of the gastrointestinal tract in individuals diagnosed as children with atypical autism: a Danish register study based on hospital diagnoses. Autism 2013;17:55-63.
37. Mouridsen SE, Rich B, Isager T. A longitudinal study of gastrointestinal diseases in individuals diagnosed with infantile autism as children. Child Care Health Dev 2010;36: 437-43.
38. Wang LW, Tancredi DJ, Thomas DW. The prevalence of gastrointestinal problems in children across the United States with autism spectrum disorders from families with multiple affected members. J Dev Behav Pediatr 2011;32:351-60.
39. Gorrindo P, Williams KC, Lee EB, Walker LS, McGrew SG, Levitt P. Gastrointestinal dysfunction in autism: parental report, clinical evaluation, and associated factors. Autism Res 2012;5:101-8.
40. Freitag CM, Staal W, Klauck SM, Duketis E, Waltes R. Genetics of autistic disorders: review and clinical implications. Eur Child Adolesc Psychiatry 2010;19:169-78.
41. Rosenberg RE, Law JK, Yenokyan G, McGready J, Kaufmann WE, Law PA. Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Arch Pediatr Adolesc Med 2009;163:907-14.
42. Hallmayer J, Cleveland S, Torres A, et al. Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry 2011;68:1095-102.
43. Patterson PH. Modeling autistic features in animals. Pediatr Res 2011;69:34R-40R.
44. Campbell DB, Buie TM, Winter H, et al. Distinct genetic risk based on association of MET in families with co-occurring autism and gastrointestinal conditions. Pediatrics 2009;123: 1018-24.
45. Russo AJ, Krigsman A, Jepson B, Wakefield A. Decreased serum hepatocyte growth factor (HGF) in autistic children with severe gastrointestinal disease. Biomark Insights 2009;4:181-90.
46. Campbell DB, D'Oronzio R, Garbett K, et al. Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann Neurol 2007;62:243-50. (Pubitemid 47525400)
47. Weiss LA, Abney M, Cook EH Jr, Ober C. Sex-specific genetic architecture of whole blood serotonin levels. Am J Hum Genet 2005;76:33-41. (Pubitemid 40023763)
48. Sutcliffe JS, Delahanty RJ, Prasad HC, et al. Allelic heterogeneity at the serotonin transporter locus (SLC6A4) confers susceptibility to autism and rigid-compulsive behaviors. Am J Hum Genet 2005;77:265-79. (Pubitemid 41022709)
49. Coutinho AM, Oliveira G, Morgadinho T, et al. Variants of the serotonin transporter gene (SLC6A4) significantly contribute to hyperserotonemia in autism. Mol Psychiatry 2004; 9:264-71. (Pubitemid 38496717)
50. Prasad HC, Steiner JA, Sutcliffe JS, Blakely RD. Enhanced activity of human serotonin transporter variants associated with autism. Philos Trans R Soc Lond B Biol Sci 2009;364: 163-73.
51. Schain RJ, Freedman DX. Studies on 5-hydroxyindole metabolism in autistic and other mentally retarded children. J Pediatr 1961;58:315-20.
52. Mulder EJ, Anderson GM, Kema IP, et al. Platelet serotonin levels in pervasive developmental disorders and mental retardation: diagnostic group differences, within-group distribution, and behavioral correlates. J Am Acad Child Adolesc Psychiatry 2004;43:491-9. (Pubitemid 38812390)
53. Veenstra-VanderWeele J, Muller CL, Iwamoto H, et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci U S A 2012;109:5469-74.
54. Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med 2009;60:355-66.
55. Costedio MM, Hyman N, Mawe GM. Serotonin and its role in colonic function and in gastrointestinal disorders. Dis Colon Rectum 2007;50:376-88. (Pubitemid 46394454)
56. Manocha M, Khan WI. Serotonin and GI disorders: an update on clinical and experimental studies. Clin Transl Gastroenterol 2012;3:e13.
57. Patterson PH. Maternal infection and immune involvement in autism. Trends Mol Med 2011;17:389-94.
58. Abdallah MW, Larsen N, Grove J, et al. Amniotic fluid chemokines and autism spectrum disorders: an exploratory study utilizing a Danish Historic Birth Cohort. Brain Behav Immun 2012;26:170-6.
59. Atladottir HO, Thorsen P, Ostergaard L, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 2010;40: 1423-30.
60. Chess S. Follow-up report on autism in congenital rubella. J Autism Child Schizophr 1977;7:69-81. (Pubitemid 8081958)
61. Goines P, Van de Water J. The immune system's role in the biology of autism. Curr Opin Neurol 2010;23:111-7.
62. Onore C, Careaga M, Ashwood P. The role of immune dysfunction in the pathophysiology of autism. Brain Behav Immun 2012;26:383-92.
63. Hsiao EY, McBride SW, Chow J, Mazmanian SK, Patterson PH. Modeling an autism risk factor in mice leads to permanent immune dysregulation. Proc Natl Acad Sci U S A 2012;109: 12776-81.
64. Rout UK, Mungan NK, Dhossche DM. Presence of GAD65 autoantibodies in the serum of children with autism or ADHD. Eur Child Adolesc Psychiatry 2012;21:141-7.
65. Braunschweig D, Van de Water J. Maternal autoantibodies in autism. Arch Neurol 2012;69:693-9.
66. Heuer L, Braunschweig D, Ashwood P, Van de Water J, Campbell DB. Association of a MET genetic variant with autism-associated maternal autoantibodies to fetal brain proteins and cytokine expression. Transl Psychiatry 2011;1:e48.
67. Bercik P. The microbiota-gut-brain axis: learning from intestinal bacteria? Gut 2011;60:288-9.
68. Mayer EA. Gut feelings: the emerging biology of gut-brain communication. Nat Rev Neurosci 2011;12:453-66.
69. Critchfield JW, van Hemert S, Ash M, Mulder L, Ashwood P. The potential role of probiotics in the management of childhood autism spectrum disorders. Gastroenterol Res Pract 2011;2011: 161358.
70. Ashwood P, Anthony A, Torrente F, Wakefield AJ. Spontaneous mucosal lymphocyte cytokine profiles in children with autism and gastrointestinal symptoms: mucosal immune activation and reduced counter regulatory interleukin-10. J Clin Immunol 2004;24:664-73. (Pubitemid 40933118)
71. Ashwood P, Wakefield AJ. Immune activation of peripheral blood and mucosal CD3+ lymphocyte cytokine profiles in children with autism and gastrointestinal symptoms. J Neuroimmunol 2006;173:126-34.
72. Jyonouchi H, Geng L, Streck DL, Toruner GA. Children with autism spectrum disorders (ASD) who exhibit chronic gastrointestinal (GI) symptoms and marked fluctuation of behavioral symptoms exhibit distinct innate immune abnormalities and transcriptional profiles of peripheral blood (PB) monocytes. J Neuroimmunol 2011;238:73-80.
73. Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Pessah I, Van de Water J. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav Immun 2011;25:40-5.
74. Heuer L, Ashwood P, Schauer J, et al. Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms. Autism Res 2008;1:275-83.
75. Garay PA, McAllister AK. Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front Synaptic Neurosci 2010;2:136.
76. Maenner MJ, Arneson CL, Levy SE, Kirby RS, Nicholas JS, Durkin MS. Brief report: association between behavioral features and gastrointestinal problems among children with autism spectrum disorder. J Autism Dev Disord 2012;42:1520-5.
77. Sajadinejad MS, Asgari K, Molavi H, Kalantari M, Adibi P. Psychological issues in inflammatory bowel disease: an overview. Gastroenterol Res Pract 2012;2012:106502.
78. Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol 2011;62:591-9.
79. Whitehead WE, Palsson O, Jones KR. Systematic review of the comorbidity of irritable bowel syndrome with other disorders: what are the causes and implications? Gastroenterology 2002;122:1140-56.
80. Tramullas M, Dinan TG, Cryan JF. Chronic psychosocial stress induces visceral hyperalgesia in mice. Stress 2012;15:281-92.
81. Julio-Pieper M, O'Mahony CM, Clarke G, Bravo JA, Dinan TG, Cryan JF. Chronic stress-induced alterations in mouse colonic 5-HT and defecation responses are strain dependent. Stress 2012;15:218-26.
82. Reber SO. Stress and animal models of inflammatory bowel disease - an update on the role of the hypothalamo-pituitaryadrenal axis. Psychoneuroendocrinology 2012;37:1-19.
83. Vicario M, Alonso C, Guilarte M, et al. Chronic psychosocial stress induces reversible mitochondrial damage and corticotropinreleasing factor receptor type-1 upregulation in the rat intestine and IBS-like gut dysfunction. Psychoneuroendocrinology 2012;37: 65-77.
84. Ghia JE, Blennerhassett P, Collins SM. Impaired parasympathetic function increases susceptibility to inflammatory bowel disease in a mouse model of depression. J Clin Invest 2008;118:2209-18. (Pubitemid 351872339)
85. Horvath K, Perman JA. Autism and gastrointestinal symptoms. Curr Gastroenterol Rep 2002;4:251-8.
86. Nikolov RN, Bearss KE, Lettinga J, et al. Gastrointestinal symptoms in a sample of children with pervasive developmental disorders. J Autism Dev Disord 2009;39:405-13.
87. Mazurek MO, Vasa RA, Kalb LG, et al. Anxiety, sensory over-responsivity, and gastrointestinal problems in children with autism spectrum disorders. J Abnorm Child Psychol 2013;41:165-76.
88. Pennesi CM, Klein LC. Effectiveness of the gluten-free, casein-free diet for children diagnosed with autism spectrum disorder: based on parental report. Nutr Neurosci 2012;15: 85-91.
89. Knivsberg AM, Reichelt KL, Hoien T, Nodland M. A randomised, controlled study of dietary intervention in autistic syndromes. Nutr Neurosci 2002;5:251-61. (Pubitemid 34823462)
90. Whiteley P, Haracopos D, Knivsberg AM, et al. The ScanBrit randomised, controlled, single-blind study of a gluten- and casein-free dietary intervention for children with autism spectrum disorders. Nutr Neurosci 2010;13:87-100.
91. Sandler RH, Finegold SM, Bolte ER, et al. Short-term benefit from oral vancomycin treatment of regressive-onset autism. J Child Neurol 2000;15:429-35. (Pubitemid 30460223)