Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified

De Angelis, Maria; Piccolo, Maria; Vannini, Lucia; Siragusa, Sonya; De Giacomo, Andrea; Serrazzanetti, Diana Isabella; Cristofori, Fernanda; Guerzoni, Maria Elisabetta; Gobbetti, Marco; Francavilla, Ruggiero

doi:10.1371/journal.pone.0076993

Cited by 887Gut microbiota and healthAutism Spectrum Disorder ResearchGastrointestinal motility and disorders

Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified

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De Angelis, Maria, Piccolo, Maria, Vannini, Lucia, Siragusa, Sonya, De Giacomo, Andrea, Serrazzanetti, Diana Isabella, Cristofori, Fernanda, Guerzoni, Maria Elisabetta +2 more·2013·PLoS ONE

DOI 10.1371/journal.pone.0076993PMC PMC3793965

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Abstract

This study aimed at investigating the fecal microbiota and metabolome of children with Pervasive Developmental Disorder Not Otherwise Specified (PDD-NOS) and autism (AD) in comparison to healthy children (HC). Bacterial tag-encoded FLX-titanium amplicon pyrosequencing (bTEFAP) of the 16S rDNA and 16S rRNA analyses were carried out to determine total bacteria (16S rDNA) and metabolically active bacteria (16S rRNA), respectively. The main bacterial phyla (Firmicutes, Bacteroidetes, Fusobacteria and Verrucomicrobia) significantly (P<0.05) changed among the three groups of children. As estimated by rarefaction, Chao and Shannon diversity index, the highest microbial diversity was found in AD children. Based on 16S-rRNA and culture-dependent data, Faecalibacterium and Ruminococcus were present at the highest level in fecal samples of PDD-NOS and HC children. Caloramator, Sarcina and Clostridium genera were the highest in AD children. Compared to HC, the composition of Lachnospiraceae family also differed in PDD-NOS and, especially, AD children. Except for Eubacterium siraeum, the lowest level of Eubacteriaceae was found on fecal samples of AD children. The level of Bacteroidetes genera and some Alistipes and Akkermansia species were almost the highest in PDD-NOS or AD children as well as almost all the identified Sutterellaceae and Enterobacteriaceae were the highest in AD. Compared to HC children, Bifidobacterium species decreased in AD. As shown by Canonical Discriminant Analysis of Principal Coordinates, the levels of free amino acids and volatile organic compounds of fecal samples were markedly affected in PDD-NOS and, especially, AD children. If the gut microbiota differences among AD and PDD-NOS and HC children are one of the concomitant causes or the consequence of autism, they may have implications regarding specific diagnostic test, and/or for treatment and prevention.

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Cross-sectional studies comparing the gut microbiota composition between healthy and ASD individuals have revealed an altered microbiota profile in patients with ASD, with several studies reporting increased levels of Clostridium and Lactobacillus along with elevated levels of SCFAs, including propionic and butyric acid.
“Cross-sectional studies comparing the gut microbiota composition between healthy and ASD individuals have revealed an altered microbiota profile in patients with ASD, with several studies reporting increased levels of Clostridium and Lactobacillus along with elevated levels of SCFAs, including propionic and butyric acid (Wang et al., 2012, 2013; De Angelis et al., 2013; Kang et al., 2013).”
From Microbiome–microglia connections via the gut–brain axis (2019) · cites this paper as De Angelis et al., 2013
Autistic children exhibit lower overall SCFA levels, with a particularly pronounced reduction in butyrate.
“Studies indicate that autistic children exhibit lower overall SCFA levels, with a particularly pronounced reduction in butyrate [50].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
SCFAs cross the blood-brain barrier and influence early brain development by regulating the production of serotonin and dopamine.
“Furthermore, SCFAs cross the BBB and influence early brain development by regulating the production of serotonin and dopamine [50,52].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
SCFAs possess neuroprotective properties and, through epigenetic modifications, enhance memory formation and neural plasticity.
“Additionally, SCFAs possess neuroprotective properties and, through epigenetic modifications, enhance memory formation and neural plasticity [49,50,55].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
An elevated abundance of Ruminococcaceae, Enterobacteriaceae, Pasteurellaceae, and Lachnospiraceae families has been observed in the digestive tract of individuals with ASD.
“Moreover, an elevated abundance of Ruminococcaceae, Enterobacteriaceae, Pasteurellaceae, and Lachnospiraceae families has been observed in the digestive tract of individuals with ASD [8,50,52,96,97,98,101,105,110,111].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]

Studies have shown a significant increase in the prevalence of Clostridium bacteria in ASD patients compared to the general population.
“Studies has shown a significant increase in the prevalence of Clostridium bacteria in ASD patients compared to the general population [8,50,52,96,97,98,99,100,101,102,103,104,105,106,107,108,109].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
Studies suggest a potential increase in the prevalence of Lactobacillus in the fecal samples of patients diagnosed with ASD.
“Additionally, studies suggest a potential increase in the prevalence of Lactobacillus in the fecal samples of patients diagnosed with ASD [8,18,50,96,97,98,102,103,106,109,110,111].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
The presence of Alistipes may be observed at elevated levels in patients diagnosed with ASD.
“Furthermore, the presence of Alistipes may be observed at elevated levels in patients diagnosed with ASD [50,89,96,97,98].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
An increasing number of studies indicate that the population of Desulfovibrio could exhibit an increase in cases of ASD.
“An increasing number of studies indicate that the population of Desulfovibrio could exhibit an increase in cases of ASD [50,96,97,98,103,106,107,109].”
From The Gut–Brain–Microbiota Connection and Its Role in Autism Spectrum Disorders (2025) · cites this paper as [50]
Abnormal tryptophan metabolism has been reported in plasma and feces of children with ASD.
“in both plasma (17) and feces (18), abnormal tryptophan metabolism has been reported in children with ASD”
From Fecal Microbiome Transplantation from Children with Autism Spectrum Disorder Modulates Tryptophan and Serotonergic Synapse Metabolism and Induces Altered Behaviors in Germ-Free Mice (2021) · cites this paper as [18]
SCFAs act in the brain via FFAR2 and FFAR3 and in the gut; in the brain they impact neurotransmitter and catecholamine production and affect reward, synaptic plasticity, and memory; in the intestine they influence water and electrolyte resorption, modulate oxidative and inflammatory state, strengthen mucosal barrier, regulate visceral sensitivity and motility, and can alter integrity of the gutand
“which are fermentation end products of non-digested carbohydrates, act both in the brain via free fatty acid receptors FFAR2 and FFAR3, and in the gut.In the brain, they have an impact on the production of neurotransmitters and catecholamines [280,282] and partially they affect the reward system, synaptic plasticity, and memory formation [286,287].In the intestine, they influence water and”
From The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders (2021) · cites this paper as [280]
Several studies found lower levels of fecal short-chain fatty acids, including butyrate, in feces of ASD children, while a 2012 study found increased ammonia and short-chain fatty acids including acetic, butyric, isobutyric, valeric, and isovaleric acids in ASD.
“Several studies found lower levels of fecal SCFA, including butyrate in feces of ASD children [53, 64], while a 2012 study found increased ammonia and SCFA including acetic, butyric, isobutyric, valeric, and isovaleric acids in ASD [61].”
From The Gut Microbiota and Dysbiosis in Autism Spectrum Disorders (2018) · cites this paper as [64]
Some studies found increased diversity of microbiota in ASD, whereas other studies show decreased diversity and richness or no differences in diversity.
“Some studies found increased diversity of the microbiota in ASD [47, 64], whereas other studies show the opposite trend towards decreased diversity and richness [73, 74], or no differences in diversity [75, 77].”
From The Gut Microbiota and Dysbiosis in Autism Spectrum Disorders (2018) · cites this paper as [64]
Metabolomic analyses of serum, feces, and urine from ASD subjects have uncovered differences in various molecules compared to TD individuals, with many dysregulated compounds being of microbial origin.
“metabolomic analyses of serum, feces, and urine from ASD subjects have uncovered differences in various molecules compared to TD individuals, with many dysregulated compounds being of microbial origin (De Angelis et al., 2013; Kang et al., 2017a; Ming et al., 2012; Mussap et al., 2016; Wang et al., 2019).”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as De Angelis et al., 2013
Gut bacterial communities differ between individuals with ASD and typically-developing controls.
“Gut bacterial communities differ between individuals with ASD and typically-developing (TD) controls (Coretti et al., 2018; De Angelis et al., 2013; Finegold et al., 2010; Gondalia et al., 2012; Kang et al., 2013, 2017a; Kushak et al., 2016; Liu et al., 2019; Son et al., 2015; Strati et al., 2017; Wang et al., 2019; Williams et al., 2011)”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as De Angelis et al., 2013
There were higher concentrations of amino acids in colon contents of oASD mice, similar to reports studying individuals with ASD.
“There were higher concentrations of amino acids in colon contents of oASD mice, similar to reports studying individuals with ASD (De Angelis et al., 2013).”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as De Angelis et al., 2013
Microbiome profiles of ASD individuals, especially those with co-morbid GI dysfunction, differ from that of TD controls.
“Since then numerous studies from diverse cohorts have reported that microbiome profiles of ASD individuals, especially those with co-morbid GI dysfunction, differ from that of TD controls (Coretti et al., 2018; De Angelis et al., 2013; Finegold et al., 2010; Gondalia et al., 2012; Kang et al., 2013, 2017a; Kushak et al., 2016; Liu et al., 2019; Son et al., 2015; Strati et al., 2017; Wang et al., 2”
From Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice (2019) · cites this paper as De Angelis et al., 2013
Two studies showed increases in alpha diversity and six studies showed no significant changes in alpha diversity.
“Two studies showed increases [31, 33] and six studies showed no significant changes in alpha diversity [36, 42, 43, 48, 50, 54].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
The rest of the studies observed either a decrease in Bacteroidetes percentage or no significant differences between cases and controls.
“The rest of the studies observed either a decrease in Bacteroidetes percentage [50, 54] or no significant differences between cases and controls [31, 36, 48].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
Among seven papers reporting beta diversity, four showed significant differences in beta diversity between ASD and SIB/HC while the rest did not.
“Among the seven [31, 36, 40–42, 48, 50] papers that reported on beta diversity, four [31, 40, 41, 50] papers showed significant differences in beta diversity between ASD and SIB/HC while the rest did not (Additional file 1: Table S2).”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
At the Firmicutes phylum level, none of the six studies showed an increase in absolute or relative abundance.
“At the phylum level, none of the six studies showed an increase in absolute or relative abundance [31, 33, 36, 48, 51, 54].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
These seven Prevotella studies showed either a non-significant result in relative abundance or a lower relative abundance in children classified as ASD versus SIB or HC.
“Instead, these seven studies showed either a non-significant result in relative abundance [41, 48, 50, 52] or a lower relative abundance in children classified as ASD versus SIB or HC [31, 39, 42].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
For relative abundance in total and metabolically active Firmicutes, studies demonstrated either a decrease or no significant differences between children with ASD, SIB, and HC.
“For relative abundance in both total and metabolically active Firmicutes, the studies demonstrated either a decrease [31, 33, 36] or no significant differences between children with ASD, SIB, and HC [48, 51, 54].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
The general trend supports no alterations in E. coli for children with ASD in five studies versus one study documenting a decrease in E. coli percentage.
“The general trend, however, supports no alterations in E. coli for children in ASD in five studies [30, 35, 42, 48, 52] vs one study [31] documenting a decrease in E. coli percentage among other microbiota.”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
Streptococcus results (not S. thermophilus) corroborated an overall decrease in counts and percentage in ASD cases when statistical significance was reached.
“In the order Lactobacillales and family Streptococcaceae, Streptococcus results (not S. thermophilus) corroborated an overall decrease in counts and percentage in ASD cases when statistical significance was reached [30, 31, 33, 37, 41].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
No specific findings were identified in the Verrucomicrobia phylum and in the Verrucomicrobiaceae family.
“No specific findings were identified in the Verrucomicrobia phylum [31, 33, 36, 39, 48] and in the Verrucomicrobiaceae family [31, 37, 39, 41, 52].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
Bifidobacterium consistently showed lower counts and proportions in children with ASD versus their siblings or controls.
“however, upon a closer look at Bifidobacterium, consistently lower counts and proportions were found in children with ASD versus their siblings [31, 52] or controls [30, 38, 47].”
From Gut microbiota changes in children with autism spectrum disorder: a systematic review (2020) · cites this paper as [31]
This study did not replicate previously reported differences in the relative abundances of bacterial categories, including the Bacteroidetes phylum, the Sutterella genus, and the Prevotella genus, between ASD and unrelated control children.
“This study did not replicate previously reported differences in the relative abundances of bacterial categories, including the Bacteroidetes phylum [12–14], the Sutterella genus [7,8,10] and the Prevotella genus [11] between ASD and unrelated control children.”
From Comparison of Fecal Microbiota in Children with Autism Spectrum Disorders and Neurotypical Siblings in the Simons Simplex Collection (2015) · cites this paper as [13]
Previous studies, with the exception of one study, failed to detect differences in microbial composition between ASD and NT siblings.
“Of note, previous studies [6–8,12,14], with the exception of one study [13], failed to detect differences in microbial composition between ASD and NT siblings [11].”
From Comparison of Fecal Microbiota in Children with Autism Spectrum Disorders and Neurotypical Siblings in the Simons Simplex Collection (2015) · cites this paper as [13]
Stool-based microbiome characterization in several cohorts identified specific genera that differed in ASD vs control subjects.
“Stool-based microbiome characterization in several cohorts identified specific genera that differed in ASD vs control subjects, but most previous studies conducted their analysis at higher taxonomic levels, with little published data at the genus or species (ie, OTU) level.22, 25, 26, 27”
From Distinct Microbiome-Neuroimmune Signatures Correlate With Functional Abdominal Pain in Children With Autism Spectrum Disorder (2017) · cites this paper as [26]
Most previous studies conducted their analysis at higher taxonomic levels, with little published data at the genus or species (OTU) level.
“Stool-based microbiome characterization in several cohorts identified specific genera that differed in ASD vs control subjects, but most previous studies conducted their analysis at higher taxonomic levels, with little published data at the genus or species (ie, OTU) level.22, 25, 26, 27”
From Distinct Microbiome-Neuroimmune Signatures Correlate With Functional Abdominal Pain in Children With Autism Spectrum Disorder (2017) · cites this paper as [26]
Other patients with ASD show the opposite result, an increased Bacteroidetes/Firmicutes ratio.
“others show the opposite result (De Angelis et al., 2013; Zhang et al., 2018)”
From Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder (2019) · cites this paper as De Angelis et al., 2013
Many children with ASD show abnormalities in GI physiology, including increased intestinal permeability, overall microbiota alterations, and gut infection with cresol-producing Clostridium difficile.
“Many ASD children have also been shown to carry abnormalities in GI physiology, including: increased intestinal permeability [34,35], overall microbiota alterations [36,37,38,39,40], and gut infection with cresol-producing Clostridium difficile [39,41,42,43,44].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [36]
Some studies revealed significant reductions in relative abundance of Prevotella, Coprococcus, Enterococcus, Lactobacillus, Streptococcus, Lactococcus, Staphylococcus, Ruminococcus, and Bifidobacterium species in children with ASD compared with healthy controls.
“Indeed, some studies have revealed significant reductions in the relative abundance of Prevotella, Coprococcus, Enterococcus, Lactobacillus, Streptococcus, Lactococcus, Staphylococcus, Ruminococcus, and Bifidobacterium species in children with ASD compared with healthy controls [36,128,143].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [36]
Several studies on ASD showed changes in the composition of the microbiota, particularly in the relative abundance of the main gut bacterial phyla.
“Several studies on ASD have showed changes in the composition of the microbiota, particularly in the relative abundance of the mains gut bacterial phyla [36,37,143,144].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [36]
Other studies observed in ASD children high abundance of Akkermansia muciniphilia, Desulfovibrio, and Faecalibacterium prausnitzii.
“Others studies observed, in ASD children, high abundance of: Akkermansia muciniphilia, [36,143,148] Desulfovibrio, [37] and Faecalibacterium prausnitzii [36].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [36]
ASD patients seem characterized by elevated SCFA concentrations in stool and serum and increased levels of SCFA-producing bacteria (e.g., Clostridia, Desulfovibrio, and Bacteroides).
“Moreover, ASD patients seem to be characterized by both elevated levels of SCFA concentrations in stool and serum, and increased level of SCFA-producing bacteria (e.g., Clostridia, Desulfovibrio, and Bacteroides) [29,36,180].”
From Autism, Gastrointestinal Symptoms and Modulation of Gut Microbiota by Nutritional Interventions (2019) · cites this paper as [36]
Decreased levels of Bifidobacterium and metabolites of free amino acids and short-chain fatty acids (SCFA) in the feces may contribute to the development of ASD.
“Decreased levels of Bifidobacterium and metabolites of free amino acids and short-chain fatty acids (SCFA) in the feces may also contribute to the development of ASD (23).”
From Association Between Gut Microbiota and Autism Spectrum Disorder: A Systematic Review and Meta-Analysis (2019) · cites this paper as [23]
In our meta-analysis, only two studies enrolled children with ASD who had no GI symptoms, and one study did not provide details about GI symptoms.
“In our meta-analysis, only two studies enrolled children with ASD who had no GI symptoms (23, 37), and one study did not provide details about GI symptoms (33).”
From Association Between Gut Microbiota and Autism Spectrum Disorder: A Systematic Review and Meta-Analysis (2019) · cites this paper as [23]
GI microbial dysbiosis has been documented in multiple studies of children with ASD.
“In addition, GI microbial dysbiosis, an imbalance in the organisms that make up the gut microbiota, has been documented in multiple studies of children with ASD [5, 7–14].”
From Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms (2019) · cites this paper as [14]
Most studies demonstrate that children with ASD have more bacterial diversity and lower overall abundance of potentially beneficial taxa such as Bifidobacterium and Akkermansia.
“Most studies demonstrate that children with ASD have more bacterial diversity [10, 14] and possess lower overall abundance of potentially beneficial taxa, such as Bifidobacterium and Akkermansia, [5, 10, 11], although some populations appear to differ from this trend [10, 13].”
From Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms (2019) · cites this paper as [14]

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Impaired Carbohydrate Digestion and Transport and Mucosal Dysbiosis in the Intestines of Children with Autism and Gastrointestinal Disturbances
Williams, B. L., Hornig, M., Buie, T., Bauman, M. L., Cho Paik, M., Wick, I., Bennett, A., Jabado, O., Hirschberg, D. L., & Lipkin, W. I. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024585 · Cited by 492 · see citing works
A vegan or vegetarian diet substantially alters the human colonic faecal microbiota
Zimmer, J., Lange, B., Frick, J.-S., Sauer, H., Zimmermann, K., Schwiertz, A., Rusch, K., Klosterhalfen, S., & Enck, P. (2012) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2011.141 · Cited by 465 · cited 1× · see citing works
“The composition of the GI microbiota is mainly influenced by genetic factors [21], age [22] and diet [23,24].”
Background
Bifidobacterial Diversity in Human Feces Detected by Genus-Specific PCR and Denaturing Gradient Gel Electrophoresis
Satokari, R. M., Vaughan, E. E., Akkermans, A. D. L., Saarela, M., & de Vos, W. M. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.2.504-513.2001 · Cited by 444 · see citing works
Low Relative Abundances of the Mucolytic Bacterium Akkermansia muciniphila and Bifidobacterium spp. in Feces of Children with Autism
Wang, L., Christophersen, C. T., Sorich, M. J., Gerber, J. P., Angley, M. T., & Conlon, M. A. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05212-11 · Cited by 432 · see citing works
Major phenylpropanoid‐derived metabolites in the human gut can arise from microbial fermentation of protein
Russell, W. R., Duncan, S. H., Scobbie, L., Duncan, G., Cantlay, L., Calder, A. G., Anderson, S. E., & Flint, H. J. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201200594 · Cited by 417 · see citing works
Role of the gut microbiota in defining human health
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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
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Effects of the enteric bacterial metabolic product propionic acid on object-directed behavior, social behavior, cognition, and neuroinflammation in adolescent rats: Relevance to autism spectrum disorder
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Voices from within: gut microbes and the CNS
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Antibiotic treatment partially protects against type 1 diabetes in the Bio-Breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes?
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Duodenal and faecal microbiota of celiac children: molecular, phenotype and metabolome characterization
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Predominant Role of Host Genetics in Controlling the Composition of Gut Microbiota
Khachatryan, Z., Ktsoyan, Z. A., Manukyan, G. P., Kelly, D., Ghazaryan, K. A., & Aminov, R. I. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003064 · Cited by 317 · see citing works
Developmental aspects of human hepatic drug glucuronidation in young children and adults
Strassburg, C. P., Strassburg, A., Kneip, S., et al. (2002) · Gut · doi:10.1136/gut.50.2.259 · Cited by 289 · see citing works
Metabolism of Linoleic Acid by Human Gut Bacteria: Different Routes for Biosynthesis of Conjugated Linoleic Acid
Devillard, E., McIntosh, F. M., Duncan, S. H., & Wallace, R. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01359-06 · Cited by 285 · see citing works
Gut microbiota: next frontier in understanding human health and development of biotherapeutics
Prakash, S., Rodes, L., Coussa-Charley, M., Tomaro-Duchesneau, C., Tomaro-Duchesneau, C., Coussa-Charley, & Rodes (2011) · Biologics · doi:10.2147/btt.s19099 · Cited by 262 · see citing works
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16S rRNA Gene Pyrosequencing Reveals Bacterial Dysbiosis in the Duodenum of Dogs with Idiopathic Inflammatory Bowel Disease
Suchodolski, J. S., Dowd, S. E., Wilke, V., Steiner, J. M., & Jergens, A. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039333 · Cited by 236 · see citing works
Recommendations for evaluation and treatment of common gastrointestinal problems in children with ASDs
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Molecular Characterisation of Gastrointestinal Microbiota of Children With Autism (With and Without Gastrointestinal Dysfunction) and Their Neurotypical Siblings
Gondalia, S. V., Palombo, E. A., Knowles, S. R., Cox, S. B., Meyer, D., & Austin, D. W. (2012) · Autism Research · doi:10.1002/aur.1253 · Cited by 208 · see citing works
Desulfovibrio species are potentially important in regressive autism
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Alteration of Plasma Glutamate and Glutamine Levels in Children with High-Functioning Autism
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Urinary p-cresol in autism spectrum disorder
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Gontcharova, V., Youn, E., Wolcott, R. D., Hollister, E. B., Gentry, T. J., & Dowd, S. E. (2010) · The Open Microbiology Journal · doi:10.2174/1874285801004010047 · Cited by 174 · see citing works
Gluten-free and casein-free diets in the treatment of autism spectrum disorders: A systematic review
Mulloy, A. M., Lang, R. B., O’Reilly, M. F., Sigafoos, J., Lancioni, G. E., & Rispoli, M. J. (2009) · Research in Autism · doi:10.1016/j.rasd.2009.10.008 · Cited by 172 · see citing works
Different Fecal Microbiotas and Volatile Organic Compounds in Treated and Untreated Children with Celiac Disease
Cagno, R. D., Rizzello, C. G., Gagliardi, F., et al. (2009) · Applied and Environmental Microbiology · doi:10.1128/aem.02793-08 · Cited by 157 · see citing works
Effect of lactose on gut microbiota and metabolome of infants with cow’s milk allergy
Francavilla, R., Calasso, M. P., Calace, L., Siragusa, S., Ndagijimana, M., Vernocchi, P., Brunetti, L. M., Mancino, G., Tedeschi, G., Guerzoni, E., et al. (2012) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2012.01286.x · Cited by 151 · see citing works
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Fontaine, J.-F., Barbosa-Silva, A., Schaefer, M., Huska, M. R., Muro, E. M., & Andrade-Navarro, M. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp353 · Cited by 147 · see citing works
Environmental risk factors for autism
Dietert, R. R., Dietert, J. M., & DeWitt, J. C. (2011) · Emerging Health Threats Journal · doi:10.3402/ehtj.v4i0.7111 · Cited by 136 · see citing works
Bifidobacterium exopolysaccharides fermented by human microbiota
Salazar, N., Fernández, M., Hernández-Barranco, A., Ruas-Madiedo, P., & Reyes-Gavilán, C. D. L. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00325-08 · Cited by 134 · see citing works
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Bifidobacterium strains suppress in vitro the pro-inflammatory milieu triggered by the large intestinal microbiota of coeliac patients
Medina, M., Palma, G. D., Ribes‐Koninckx, C., Calabuig, M., & Sanz, Y. (2008) · Journal of Inflammation · doi:10.1186/1476-9255-5-19 · Cited by 128 · see citing works
Microbial ecosystems therapeutics: a new paradigm in medicine?
Petrof, E., Claud, E. C., Gloor, G. B., & Allen‐Vercoe, E. (2012) · Beneficial Microbes · doi:10.3920/bm2012.0039 · Cited by 124 · see citing works
Hypoactivity of the central dopaminergic system and autistic-like behavior induced by a single early prenatal exposure to lipopolysaccharide
Kirsten, T. B., Chaves‐Kirsten, G. P., Chaible, L. M., Silva, A. C., Martins, D. O., Britto, L. R. G., Dagli, M. L. Z., Torrão, A. S., Palermo‐Neto, J., & Bernardi, M. M. (2012) · Journal of Neuroscience Research · doi:10.1002/jnr.23089 · Cited by 122 · see citing works
Therapy and epidemiology of autism–clostridial spores as key elements
Finegold, S. M. (2007) · Medical Hypotheses · doi:10.1016/j.mehy.2007.07.019 · Cited by 116 · see citing works
State of the art; microbiology in health and disease. Intestinal bacterial flora in autism
Finegold, S. M. (2011) · Anaerobe · doi:10.1016/j.anaerobe.2011.03.007 · Cited by 116 · see citing works
The active human gut microbiota differs from the total microbiota
Peris-Bondia, F., Latorre, A., Artacho, A., Moya, A., & D'Auria, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022448 · Cited by 113 · see citing works
A review of the life history, invasion process, and potential management of Clavelina lepadiformis Müller, 1776: a recent invasion of the northwest Atlantic
Reinhardt, J., & Hudson, D. M. (2012) · Management of Biological Invasions · doi:10.3391/mbi.2012.3.1.01 · Cited by 94 · see citing works
Characterization of enzymes involved in formation of ethyl esters of long-chain fatty acids in humans
Diczfalusy, M. A., Björkhem, I., Einarsson, C., Hillebrant, C.-G., & Alexson, S. E. H. (2001) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)31590-x · Cited by 91 · see citing works
Polysaccharide degradation by human intestinal bacteria during growth under multi-substrate limiting conditions in a three-stage continuous culture system
Macfarlane, S., Quigley, M. E., Hopkins, M. J., Newton, D. F., & Macfarlane, G. T. (1998) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1998.tb00508.x · Cited by 89 · see citing works
Hypothesis for a systems connectivity model of autism spectrum disorder pathogenesis: Links to gut bacteria, oxidative stress, and intestinal permeability
Heberling, C., Dhurjati, P., & Sasser, M. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.11.044 · Cited by 88 · see citing works
Does the Human Gut Microbiota Contribute to the Etiology of Autism Spectrum Disorders?
Louis, P. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2286-1 · Cited by 81 · see citing works
Acid Stress-Mediated Metabolic Shift in Lactobacillus sanfranciscensis LSCE1
Serrazanetti, D. I., Ndagijimana, M., Sado-Kamdem, S. L., Corsetti, A., Vogel, R. F., Ehrmann, M. A., & Guerzoni, M. E. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.01826-10 · Cited by 76 · see citing works
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Nutrition in inflammatory bowel disease
Razack, R., & Seidner, D. L. (2007) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e3281ddb2a3 · Cited by 70 · see citing works
Harnessing the power of the human microbiome
Blaser, M. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002112107 · Cited by 67 · see citing works
Effect of a synbiotic food consumption on human gut metabolic profiles evaluated by 1H Nuclear Magnetic Resonance spectroscopy
Ndagijimana, M., Laghi, L., Vitali, B., Placucci, G., Brigidi, P., & Guerzoni, M. E. (2009) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2009.04.016 · Cited by 64 · see citing works
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Genome‐scale metabolic model integrated with RNAseq data to identify metabolic states of Clostridium thermocellum
Gowen, C. M., & Fong, S. S. (2010) · Biotechnology Journal · doi:10.1002/biot.201000084 · Cited by 52 · see citing works
A Microbial Association with Autism
Benach, J. L., Li, E., & McGovern, M. M. (2012) · mBio · doi:10.1128/mbio.00019-12 · Cited by 41 · see citing works
Riboswitches for Intracellular Study of Genes Involved inFrancisellaPathogenesis
Reynoso, C. M. K., Miller, M. A., Bina, J. E., et al. (2012) · mBio · doi:10.1128/mbio.00253-12 · Cited by 34 · see citing works
Imitation and communication skills development in children with pervasive developmental disorders
Margari, L., GIACOMO, A. D., Portoghese, C., Martinelli, D., Fanizza, I., & L’Abate, L. (2009) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s5679 · Cited by 18 · see citing works
Faecal microbiota of individuals with autism spectrum disorder
Gondalia, S. V., Palombo, E. A., Knowles, S. R., & Austin, D. (2010) · E-Journal of Applied Psychology · doi:10.7790/ejap.v6i2.213 · Cited by 14 · see citing works
Obesity and Colorectal Cancer Risk: Impact of the Gut Microbiota and Weight-Loss Diets
Flint, H. J., & Wallace, R. J. (2010) · The Open Obesity Journal · doi:10.2174/1876823701002010050 · Cited by 7 · see citing works
Obesity and Colorectal Cancer Risk: Impact of the Gut Microbiota and Weight-Loss Diets~!2009-09-07~!2009-09-23~!2010-07-13~!
Flint, H. J., & Wallace, R. J. (2010) · The Open Obesity Journal · doi:10.2174/1876823701002020050 · Cited by 3 · see citing works
Influence of gut microbiota and manipulation by probiotics and prebiotics on host tissue fat: Potential clinical implications
Wall, R., Ross, R. P., Shanahan, F., et al. (2012) · Lipid Technology · doi:10.1002/lite.201200232 · Cited by 3 · see citing works

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Gut microbiota are related to Parkinson's disease and clinical phenotype
Scheperjans, F., Aho, V., Pereira, P. A. B., Koskinen, K., Paulin, L., Pekkonen, E., Haapaniemi, E., Kaakkola, S., Eerola‐Rautio, J., Pohja, M., et al. (2015) · Movement Disorders · doi:10.1002/mds.26069 · Cited by 1,968 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
High-level adherence to a Mediterranean diet beneficially impacts the gut microbiota and associated metabolome
De Filippis, F., Pellegrini, N., Vannini, L., Jeffery, I. B., La Storia, A., Laghi, L., Serrazanetti, D. I., Di Cagno, R., Ferrocino, I., Lazzi, C., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309957 · Cited by 1,638 · see citing works
Self-citation
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
Microbiota Transfer Therapy Alters Gut Ecosystem and Improves Gastrointestinal and Autism Symptoms: An Open-Label Study
Kang, D.-W., Adams, J. B., Gregory, A. C., Borody, T., Chittick, L., Fasano, A., Khoruts, A., Geis, E., Maldonado, J., McDonough-Means, S., et al. (2017) · Microbiome · doi:10.1186/s40168-016-0225-7 · Cited by 1,391 · see citing works
How informative is the mouse for human gut microbiota research?
Nguyen, T. L. A., Vieira-Silva, S., Liston, A., & Raes, J. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.017400 · Cited by 1,334 · see citing works
“…brain function, through neurohumoral communication (dubbed the gut-brain axis) have also been gaining attention in gastrointestinal disorders, such as irritable bowel syndrome, as well as in more unexpected pathologies, such as autism (De Angelis et al., 2013; Kang et al., 2013; Wang et al., 2013).”
Background
Alterations of the human gut microbiome in multiple sclerosis
Jangi, S., Gandhi, R., Cox, L. M., Li, N., von Glehn, F., Yan, R., Patel, B., Mazzola, M. A., Liu, S., Glanz, B. L., et al. (2016) · Nature Communications · doi:10.1038/ncomms12015 · Cited by 1,307 · see citing works
Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice
Sharon, G., Cruz, N. J., Kang, D.-W., Gandal, M. J., Wang, B., Kim, Y.-M., Zink, E. M., Casey, C. P., Taylor, B. C., Lane, C. J., et al. (2019) · Cell · doi:10.1016/j.cell.2019.05.004 · Cited by 1,182 · see citing works
Impacts of gut bacteria on human health and diseases
Zhang, Y.-J., Li, S., Gan, R.-Y., Zhou, T., Xu, D.-P., & Li, H.-B. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16047493 · Cited by 1,055 · see citing works
Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder
Sgritta, M., Dooling, S. W., Buffington, S. A., Momin, E. N., Francis, M. B., Britton, R. A., & Costa-Mattioli, M. (2019) · Neuron · doi:10.1016/j.neuron.2018.11.018 · Cited by 865 · see citing works
The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders
Socała, K., Doboszewska, U., Szopa, A., Serefko, A., Włodarczyk, M., Zielińska, A., Poleszak, E., Fichna, J., & Wlaź, P. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105840 · Cited by 857 · see citing works
Gut microbiota depletion from early adolescence in mice: implications for brain and behaviour
Desbonnet, L., Clarke, G., Traplin, A., O’Sullivan, O., Crispie, F., Moloney, R. D., Cotter, P. D., Dinan, T. G., & Cryan, J. F. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.04.004 · Cited by 760 · see citing works
Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota
Kang, D.-W., Adams, J. B., Coleman, D. M., Pollard, E. L., Maldonado, J., McDonough-Means, S., Caporaso, J. G., & Krajmalnik-Brown, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-42183-0 · Cited by 749 · see citing works
The Gut Microbiome and the Brain
Galland, L. (2014) · Journal of Medicinal Food · doi:10.1089/jmf.2014.7000 · Cited by 648 · see citing works
Autism Spectrum Disorders and the Gut Microbiota
Fattorusso, A., Di Genova, L., Dell’Isola, G., Mencaroni, E., & Esposito, S. (2019) · Nutrients · doi:10.3390/nu11030521 · Cited by 484 · see citing works
Microbiome–microglia connections via the gut–brain axis
Abdel-Haq, R., Schlachetzki, J. C. M., Glass, C. K., & Mazmanian, S. K. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20180794 · Cited by 471 · see citing works
Altered gut microbiota and short chain fatty acids in Chinese children with autism spectrum disorder
Liu, S., Li, E., Sun, Z., Fu, D., Duan, G., Jiang, M., Yu, Y., Mei, L., Yang, P., Tang, Y., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-36430-z · Cited by 457 · see citing works
Microbiota-derived metabolites as drivers of gut–brain communication
Ahmed, H., Leyrolle, Q., Koistinen, V., Kärkkäinen, O., Layé, S., Delzenne, N., & Hanhineva, K. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2102878 · Cited by 462 · see citing works
The Gut Microbiota and Autism Spectrum Disorders
Li, Q., Han, Y., Dy, A. B. C., & Hagerman, R. J. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00120 · Cited by 462 · see citing works
Altered gut microbiota and activity in a murine model of autism spectrum disorders
de Theije, C. G. M., Wopereis, H., Ramadan, M., van Eijndthoven, T., Lambert, J., Knol, J., Garssen, J., Kraneveld, A. D., & Oozeer, R. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.005 · Cited by 433 · see citing works
Gut Microbiota Profiling: Metabolomics Based Approach to Unravel Compounds Affecting Human Health
Vernocchi, P., Del Chierico, F., & Putignani, L. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01144 · Cited by 426 · see citing works
The progress of gut microbiome research related to brain disorders
Zhu, S., Jiang, Y., Xu, K., Cui, M., Ye, W., Zhao, G., Jin, L., & Chen, X. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1705-z · Cited by 419 · see citing works
Fecal Microbiota Transplantation in Neurological Disorders
Vendrik, K. E. W., Ooijevaar, R. E., de Jong, P. R. C., Laman, J. D., van Oosten, B. W., van Hilten, J. J., Ducarmon, Q. R., Keller, J. J., Kuijper, E. J., & Contarino, M. F. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00098 · Cited by 413 · see citing works
The Possible Role of the Microbiota-Gut-Brain-Axis in Autism Spectrum Disorder
Srikantha, P., & Mohajeri, M. H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092115 · Cited by 400 · see citing works
Differences in fecal microbial metabolites and microbiota of children with autism spectrum disorders
Kang, D.-W., Ilhan, Z. E., Isern, N. G., Hoyt, D. W., Howsmon, D. P., Shaffer, M., Lozupone, C. A., Hahn, J., Adams, J. B., & Krajmalnik-Brown, R. (2018) · Anaerobe · doi:10.1016/j.anaerobe.2017.12.007 · Cited by 381 · see citing works
It's all relative: analyzing microbiome data as compositions
Gloor, G. B., Wu, J. R., Pawlowsky-Glahn, V., & Egozcue, J. J. (2016) · Annals of Epidemiology · doi:10.1016/j.annepidem.2016.03.003 · Cited by 323 · see citing works
Composition of gut microbiota in children with autism spectrum disorder: a systematic review and meta-analysis
Iglesias-Vázquez, L., Van Ginkel Riba, G., Arija, V., & Canals, J. (2020) · Nutrients · doi:10.3390/nu12030792 · Cited by 352 · see citing works
Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism
Golubeva, A. V., Joyce, S. A., Moloney, G., Burokas, A., Sherwin, E., Arboleya, S., Flynn, I., Khochanskiy, D., Moya-Pérez, A., Peterson, V., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.09.020 · Cited by 364 · see citing works
Probiotics and fructo-oligosaccharide intervention modulate the microbiota-gut brain axis to improve autism spectrum reducing also the hyper-serotonergic state and the dopamine metabolism disorder
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Authors: De Angelis, M., Piccolo, M., Vannini, L., Siragusa, S., De Giacomo, A., Serrazzanetti, D. I., Cristofori, F., Guerzoni, M. E., Gobbetti, M., & Francavilla, R.
Affiliations: University of Bologna (IT)
University of Bari Aldo Moro (IT)
ORCID: Vannini, Lucia
Cristofori, Fernanda
Gobbetti, Marco
Francavilla, Ruggiero
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2013-10-09
Volume: 8
Issue: 10
Pages: e76993
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0076993
PMC: PMC3793965
OpenAlex: W2144133378
Cited by: 887
References: 82
Citations by year: 2026: 43 · 2025: 68 · 2024: 69 · 2023: 104 · 2022: 98 · 2021: 125 · 2020: 85 · 2019: 76 · 2018: 70 · 2017: 35 · 2016: 52 · 2015: 37 · 2014: 23 · 2013: 1
FWCI: 16.86
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion)
Open Research (University of Surrey) (submittedVersion, other-oa)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Keywords: autism spectrum disorder, pervasive developmental disorder not otherwise specified, gut microbiota, fecal metabolome, children, microbial diversity, Firmicutes, Bacteroidetes, Faecalibacterium, Ruminococcus, Lachnospiraceae, Akkermansia, Bifidobacterium, free amino acids, volatile organic compounds, 16S rRNA, 16S rRNA gene
MeSH terms: Amino Acids, Autistic Disorder, Bacteria, Child, Child Development Disorders, Pervasive, Child, Preschool, Feces, Female, Humans, Male, Sequence Analysis, Metabolome, Volatile Organic Compounds, Microbiota

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Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified

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