Analysis of the Duodenal Microbiome in Autistic Individuals: Association with Carbohydrate Digestion

Journal of Pediatric Gastroenterology and Nutrition

Volumn 64, Issue 5, 2017, Pages e110-e116

  Kushak, Rafail I ^a   Winter, Harland S ^a   Buie, Timothy M ^a   Cox, Stephen B ^b   Phillips, Caleb D ^b,c   Ward, Naomi L ^d,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Research and Testing Laboratory   (United States)

^c TEXAS TECH UNIVERSITY   (United States)

^d Department of Molecular Biology ^*  (United States)

^e UNIVERSITY OF WYOMING   (United States)

Author keywords

autism; duodenum; intestinal disaccharidases; microbiota

Indexed keywords

ALPHA GLUCOSIDASE; CARBOHYDRATE; DISACCHARIDASE; RNA 16S; SUCRASE; BIOLOGICAL MARKER;

ADOLESCENT; ARTICLE; ASSOCIATION; AUTISM; BACTERIAL GROWTH; BACTEROIDES; BURKHOLDERIA; CARBOHYDRATE ABSORPTION; CARBOHYDRATE INTOLERANCE; CLINICAL ARTICLE; CONSTIPATION; CONTROLLED STUDY; DIGESTION; DUODENUM MUCOSA; DYSBIOSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; FEMALE; GASTROESOPHAGEAL REFLUX; GASTROINTESTINAL SYMPTOM; GENE SEQUENCE; HUMAN; INTESTINE FLORA; MALE; MICROBIAL DIVERSITY; NEISSERIA; PRIORITY JOURNAL; ULCERATIVE COLITIS; CARBOHYDRATE METABOLISM; CASE CONTROL STUDY; COMPLICATION; DIET; DUODENUM; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; RETROSPECTIVE STUDY; STATISTICAL MODEL;

ADOLESCENT; AUTISTIC DISORDER; BIOMARKERS; CARBOHYDRATE METABOLISM; CASE-CONTROL STUDIES; DIET; DIGESTION; DISACCHARIDASES; DUODENUM; DYSBIOSIS; FEMALE; GASTROINTESTINAL MICROBIOME; HUMANS; INTESTINAL MUCOSA; LINEAR MODELS; MALE; MICROBIOTA; RETROSPECTIVE STUDIES;

EID: 84994234321     PISSN: 02772116     EISSN: 15364801     Source Type: Journal    
DOI: 10.1097/MPG.0000000000001458     Document Type: Article

References (46)

1. Buie T, Campbell DB, Fuchs GJ, et al. Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: a consensus report. Pediatrics 2010;125:1-18.
2. Hatheway CL. Toxigenic clostridia. Clin Microbiol Rev 1990;3:66-98.
3. Bolte ER. Autism and Clostridium tetani. Med Hypotheses 1998;51: 133-44.
4. Finegold SM, Molitoris D, Song Y, et al. Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002;35(suppl 1):S6-16.
5. Song Y, Liu C, Finegold SY. Real-time PCR quantification of clostridia in feces of autistic children. Appl Environ Micobiol 2004;70: 6459-65.
6. Parracho HM, Bingham MO, Gibson GR, et al. Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. J Med Microbiol 2005;54:987-91.
7. Finegold SM, Dowd SE, Gontcharova V, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010; 16:444-53.
8. Wang L, Angley MT, Gerber JP, et al. A review of candidate urinary biomarkers for autism spectrum disorder. Biomarkers 2011;16:537-52.
9. Kang DW, Park JG, Ilhan ZE, et al. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS One 2013;3:e68322.
10. Adams JB, Johansen LJ, Powell LD, et al. Gastrointestinal flora and gastrointestinal status in children with autism-comparisons to typical children and correlation with autism severity. BMC Gastroenterol 2011;11:22.
11. Simon GL, Gorbach SL. The human intestinal microflora. Dig Dis Sci 1986;31:147-62.
12. Riordan SM, McIver CJ, Wakefield D, et al. Small intestinal mucosal immunity and morphometry in luminal overgrowth of indigenous gut flora. Am J Gastroenterol 2001;96:494-500.
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. Wang L, Christophersen CT, Sorich MJ. Elevated fecal short chain fatty acid and ammonia concentrations in children with autism spectrum disorder. Dig Dis Sci 2012;57:2096-102.
15. Williams BL, Hornig M, Parekh T, et al. Application of novel PCRbased methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. MBio 2012;3:e00261-311
16. Kushak R, Buie T, Cox SB, et al. Analysis of the duodenal microbiome in children with autism. Gastroenterology 2014;146(5 suppl 1):S347.
17. Dahlqvist A. Assay of intestinal disaccharidases. Anal Biochem 1968;22:99-107.
18. Bradford MM. A refined and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54.
19. Belmont JW, Reid B, Taylor W, et al. Congenital sucrase-isomaltase deficiency presenting with failure to thrive, hypercalcemia, and nephrocalcinosis. BMC Pediatr 2002;2:4.
20. Pfeffecorn MD, Fitzgerald JF, Croffie JM, et al. Lactase deficiency: not more common in pediatric patients with inflammatory bowel disease than in patients with chronic abdominal pain. J Pediatr Gastroenterol Nutr 2002;35:339-43.
21. Callaway TR, Dowd SE, Edrington T, et al. Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. J Anim Sci 2010;88:3977-83.
22. Handl S, Dowd SE, Garcia-Mazcorro JF, et al. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol 2011;76:301-10.
23. Brosius J, Palmer ML, Kennedy PJ, et al. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 1978;75:4801-5485.
24. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460-1.
25. Edgar RC, Haas BJ, Clemente JC, et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194-200.
26. McDonald D, Price MN, Goodrich J, et al. An improved green genes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012;6:610-8.
27. Chao A. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 1987;43:783-91.
28. Shannon CE. A mathematical theory of communication. Bell Syst Tech J 1948;27:379-423 and 623-656.
29. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71:8228-35.
30. R. Development Core Team. R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2011.
31. Oksanen J, Blanchet FG, Kindt GB, et al. Vegan: community ecology package. R package version 2.4-1. 2016. https://CRAN.R-project.org/ package=vegan. Accessed November 7, 2016.
32. Anders S, HuberW. Differential expression analysis for sequence count data. Genome Biol 2010;11:R106.
33. Roberts DW. Labdsv: ordination and multivariate analysis for ecology. R package version 1.8-0. 2016. https://CRAN.R-project.org/package= labdsv. Accessed November 7, 2016.
34. Giamarellos-Bourboulis E, Tang J, Pyleris E. Molecular assessment of differences in the duodenal microbiome in subjects with irritable bowel syndrome. Scand J Gastroenterol 2015;50:1076-87.
35. Nistal E, Caminero A, Herrán AR, et al. Study of duodenal bacterial communities by 16s rRNA gene analysis in adults with active celiac disease versus non celiac disease controls. J Appl Microbiol 2016;120: 1691-700.
36. Schulz C, Schütte K, Malfertheiner P. Helicobacter pylori and other gastric microbiota in gastroduodenal pathologies. Dig Dis 2016; 34:210-6.
37. Ibrahim SH, Voigt RG, Katusic SK, et al. Incidence of gastrointestinal symptoms in children with autism: a population-based study. Pediatrics 2009;124:680-6.
38. Gondalia SV, Palombo EA, Knowles SR, et al. Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings. Autism Res 2012;5:419-27.
39. DeMoraes JG,Motta ME, BeltraõMF, et al. Fecal microbiota and diet of children with chronic constipation. Int J Pediatr 2016;2016: 6787269.
40. Son JS, Zheng LJ, Rowehl LM, et al. Comparison of fecal microbiota in children with autism spectrum disorders and neurotypical siblings in the simons simplex collection. PLoS One 2015;10:e0137725.
41. Kushak R, Lauwers G, Winter H, et al. Intestinal disaccharidases activity in patients with autism: effect of age, gender, and intestinal inflammation. Autism 2011;15:285-94.
42. Mielcarek C, Romond PC, Romond MB, et al. Modulation of bacterial translocation in mice mediated through lactose and human milk oligosaccharides. Anaerobe 2011;17:361-6.
43. HorvathK, Papadimitriou JC, Rabsztyn A, et al. Gastrointestinal abnormalities in children with autistic disorder. J Pediatr 1999;135:559-63.
44. Reddy BS, Wostmann BS. Intestinal disaccharidase activities in the growing germfree and conventional rats. Arch Biochem Biophys 1966;113:609-16.
45. Whitt DD, Savage DC. Kinetics of changes induced by indigenous microbiota in the activity levels of alkaline phosphatase and disaccharidases in small intestinal enterocytes in mice. Infect Immun 1980; 29:144-51.
46. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014;505:559-63.