Gut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders
Abstract
:1. Introduction
2. Materials and Methods
3. Results
3.1. Gut Bacterial Profiles in Children with Autism Spectrum Disorder
3.2. Gut Bacterial Profiles in Children and Adolescents with Attention-Deficit/Hyperactivity Disorder
3.3. Gut Bacterial Profiles in Children with Rett Syndrome
3.4. Gut Bacterial Profiles in Children and Adolescents with Anorexia Nervosa
3.5. Gut Bacterial Profiles in Adolescents with Depression
3.6. Gut Bacterial Profiles in Children with Tic Disorders
Ref. No | Study | Year | Country | Sample Size | Gender % M/F | Mean Age in Years | Mean BMI | Diagnostic Tool Patients Controls | Sample Storage | Medication Use * | Dietary Questionnaire | Evaluation of GIT Symptoms | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
ASD + PDD − NOS | |||||||||||||
[19] | Cao et al. | 2021 | China | ASD: 45 HC: 41 | ASD: 80/20 HC: 82.9/17.1 | ASD: 6.8 HC: 5.2 | ASD: 16.6 HC: 15.2 | AMSE CARS CABS DSM-5 | Psychiatric evaluation ASD psychometric tests | Microbial preservation solution was used, samples stored at room temperature | No ATB, probiotic or psychiatric medication prior sample collection | N/A | N/A |
[25] | Kang et al. | 2018 | USA | ASD: 23 HC: 21 | ASD: 95.7/4.3 HC: 71.4/28.6 | ASD: 8.4 HC: 10.1 | N/A | ATEC PDD-BI | N/A | −80 °C | No ATB or antifungal drugs 1 month prior sample collection | yes | 6-GSI |
[26] | Carissimi et al. | 2019 | Italy | ASD: 30 HC: 14 | ASD: 96.7/3.3 HC: 50/50 | Median age ASD: 3 HC: 10 | N/A | DSM-5 ADOS-2 GMDS | N/A | −80 °C | No ATB, probiotic or prebiotic 2 weeks prior sample collection | N/A | GIH |
[27] | Liu et al. | 2019 | China | ASD: 30 HC: 20 | ASD: 83/17 HC: 80/20 | ASD: 4.4 HC: 4.3 | N/A | DSM-5 ICD-10 | N/A | −80 °C | No ATB, probiotic, prebiotic or antifungal drugs 3 months prior sample collection | Participants with special diets excluded | 6-GSI |
[28] | Ma et al. | 2019 | China | ASD: 45 HC: 45 | ASD: 86.7/13.3 HC: 86.7/13.3 | ASD: 7.0 HC: 7.3 | N/A | DSM-5 CARS | N/A | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection | 79-item food frequency questionnaire | N/A |
[29] | Wang et al. | 2019 | China | ASD: 43 HC: 31 | ASD: 83.7/16.3 HC: 54.8/45.2 | ASD: 4.5 HC: 3.1 | N/A | DSM-5 | No psychiatric disorder | −80 °C | N/A | yes | Rome IV |
[30] | Dan et al. | 2020 | China | ASD: 143 HC: 143 | ASD: 90.9/9.1 HC: 88.8/11.2 | ASD: 4.9 HC: 5.2 | N/A | DSM-5 | No serious psychiatric disorder | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection, no use of AIDs or antioxidant drugs | N/A | Rome IV |
[31] | Kang et al. | 2013 | USA | ASD: 20 HC: 20 | ASD: 90/10 HC: 85/15 | ASD: 6.7 HC: 8.3 | N/A | ADOS ADI-R ATEC PDD-BI | N/A | −80 °C | No ATB or antifungal drugs 1 month prior sample collection, probiotic and nutrient use recorded | Special diets and seafood consumption recorded | 6-GSI |
[32] | Chen et al. | 2021 | China | ASD: 138 HC: 60 | ASD: 84.8/15.2 HC: 45/55 | ASD: 6.1 HC: 6.7 | N/A | ADOS CARS DSM-5 WISC-R WPPSI | Gesell development scales | −80 °C | No ATB 1 month prior sample collection | N/A | GSI |
[33] | Vernocchi et al. | 2022 | Italy | ASD: 41 HC: 35 | ASD: 87.8/12.2 HC: 60/40 | ASD: 6.5 HC: 8 | ASD: 16.5 HC: 15.8 | DSM-5 ADOS-2 ADI-R CBCL IQ/DQ tests | N/A | −80 °C | ATB, probiotic and psychiatric medication recorded | Specific diets recorded | Rome IV |
[34] | Wong et al. | 2022 | China | ASD: 92 HC: 112 | ASD: 100/0 HC: 100/0 | ASD: 8.4 HC: 8.1 | N/A | DSM-5 AQ-10 SDQ SCAS-P | AQ-10 SDQ SCAS-P | −80 °C | No ATB or regular probiotic use 1 month prior sample collection, use of psychiatric medication recorded | yes 7 day food record | R4PDQ |
[35] | Finegold et al. | 2010 | USA | ASD: 33 SIB: 7 HC: 8 | ASD: 72.7/27.3 SIB: 28.6/71.4 HC: 62.5/37.5 | Age range 2–13 | N/A | Authors’ evaluation of social, language, sensory and behaviour impairment | N/A | −80 °C | No probiotic or ATB 1 month prior sample collection | Special diets recorded | yes |
[36] | Coretti et al. | 2018 | Italy | ASD: 11 HC: 14 | ASD: 81.8/18.2 HC: 57.1/42.9 | ASD: 1.5 HC: 1.5 | N/A | DSM-5 ADOS-2 ADI-R GMDS VABS CARS | N/A | −80 °C | No ATB, probiotic, prebiotic or synbiotic 1 month prior sample collection | 3 days diet diary | Rome III |
[37] | Li et al. | 2019 | China | ASD: 59 HC: 30 | ASD: 84.7/15.3 HC: 66.7/33.3 | ASD: 4 HC: 5 | N/A | DSM-5 ADOS ABC | N/A | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection, no AIDs or antioxidant drugs | N/A | yes |
[38] | Zhai et al. | 2019 | China | ASD: 78 HC: 58 | ASD: 71.8/28.2 HC: 53.4/46.6 | ASD: 5.0 HC: 4.9 | N/A | DSM-4-TR ICD-10 ATEC | No history of ASD or neurological diseases | −80 °C | No ATB for 1 month prior sample collection, no probiotic or prebiotic | N/A | Participants with GI symptoms excluded |
[39] | Ding et al. | 2020 | China | ASD: 77 HC: 50 | ASD: 76.6/23.4 HC: 78/22 | ASD: 1.6 HC: 1.8 | N/A | DSM-5 CARS Social life ability scale, Gessel Develop. Schedules WISC | N/A | −80 °C | No ATB, probiotic or prebiotic 1 month prior sample collection | yes | N/A |
[40] | Zou et al. | 2020 | China | ASD: 48 HC: 48 | ASD: 79.2/20.8 HC: 50/50 | ASD: 5 HC: 4 | ASD: 17.4 HC: 16.3 | DSM-4 ADI-R CGI-S ABC-I | No serious psychiatric disorder | −80 °C | No ATB or probiotic prior sample collection | N/A | N/A |
[41] | Ye et al. | 2021 | China | ASD: 71 HC: 18 | ASD: 100/0 HC: 100/0 | ASD: 4.3 HC: 4.6 | N/A | ABC DSM-5 | ABC DSM-5 | −80 °C | No ATB or probiotic 1 month prior sample collection, no AIDs or antioxidant drugs in HC group | N/A | N/A |
[42] | De Angelis et al. | 2013 | Italy | ASD: 10 PDD: 10 SIB: 10 | 46.7/53.3 in all participants | Age range 4–10 | N/A | ADOS ADI-R CARS | N/A | −80 °C | No ATB, probiotic or prebiotic 1 month prior sample collection | N/A | Participants with GI symptoms excluded |
[43] | Niu et al. | 2019 | China | ASD: 114 HC: 40 | ASD: 83.3/16.7 HC: 50/50 | ASD: 4.5 HC: 4.2 | N/A | DSM-5 ATEC | N/A | N/A | No ATB, probiotic or other GI treatment 1 month prior sample collection | N/A | yes |
[44] | Zurita et al. | 2020 | Ecuador | ASD: 25 HC: 34 | ASD: 96/4 HC: 91.4/8.6 | ASD: 8.9 HC: 8.5 | N/A | ADI-R | SCQ | −80 °C | No ATB or steroids 2 weeks prior sample collection | 24-h dietary record | N/A |
[45] | Fujishiro et al. | 2022 | Japan | ASD: 7 HC: 9 | ASD: 71.4/28.6 HC: 66.7/33.3 | ASD: 10.1 HC: 14.6 | N/A | WISC-IV Denver-II ASSQ M-CHAT Paediatric and Psychological evaluation | WISC-IV Denver-II ASSQ M-CHAT Paediatrician and Psychological evaluation | −80 °C | N/A | yes | yes |
[46] | Wan et al. | 2022 | China | ASD: 64 HC: 64 | ASD: 82.8/17.2 HC: 84.4/15.6 | Median age ASD: 2.5 HC: 2.3 | N/A | DSM-4 DSM-5 | SRS-2 | N/A | No ATB, antifungal drugs, probiotic or prebiotic 2 months prior sample collection | 3 day food record Food frequency questionnaire | N/A |
[47] | Gondalia et al. | 2012 | Australia | ASD: 51 HC: 53 | ASD: 82.4/17.6 HC: 35.8/64.2 | Age range 2–12 | N/A | Psychiatrist, psychologist evaluation CARS | N/A | −20 °C | No ATB or antifungal drugs 15 days prior sample collection, probiotic use recorded | N/A | yes |
[48] | Son et al. | 2015 | USA | ASD: 59 SIB: 44 | ASD: 88/12 SIB: 48/52 | ASD: 10.3 SIB: 10.0 | N/A | ADOS CBCL | CBCL | −80 °C | No ATB or probiotic 1 month prior sample collection | One-week food/calorie count diary Special diets recorded | QPGS-RIII SSC |
[49] | Strati et al. | 2017 | Italy | ASD: 40 HC: 40 | ASD: 77.5/22.5 HC: 70/30 | ASD: 11.1 HC: 9.2 | N/A | DSM-5 ADOS ABC CARS | N/A | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection, no use of AIDs or antioxidant drugs | N/A | Rome III |
[50] | Berding et al. | 2018 | USA | ASD: 26 HC: 32 | ASD: 73.1/26.9 HC: 59.4/40.6 | ASD: 4.1 HC: 4.8 | ASD M: 16.8 ASD F: 15.1 HC M: 16.3 HC F: 16.8 | PDDBI-SV | N/A | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection, no routine medication | YAQ 3-day food diary Patients with special diet excluded | 6-GSI Bristol stool chart |
[51] | Pulikkan et al. | 2018 | India | ASD: 30 HC: 24 | ASD: 93.3/6.7 † HC: 62.5/37.5 | Median age ASD: 9.5 HC: 9.5 | Median BMI ASD: 14.78 HC: 15.79 | CARS INDT-ASD ISAA | Paediatric evaluation | −80 °C | No ATB, AIDs or antioxidant 1 month prior sample collection | 7 days diet diary No gluten-free diet | yes |
[52] | Zhang et al. | 2018 | China | ASD: 35 HC: 6 | ASD: 82.9/17.1 HC: 83.3/16.7 | ASD: 4.9 HC: 4.6 | N/A | DSM-5 | Medical evaluation Parent interview | −80 °C | No ATB, probiotic, prebiotic or APs 1 month prior sample collection | Participants with special diets excluded | N/A |
[53] | Ahmed et al. | 2020 | Egypt | ASD: 41 SIB: 45 HC: 45 | ASD: 68.3/31.7 SIB: 48.9/51.1 HC: 62.2/37.8 | ASD: 5.6 SIB: 4.3 HC: 5.4 | N/A | DSM-5 CARS | N/A | −80 °C | No probiotic before sample collection | yes | 6-GSI |
[54] | Ha et al. | 2021 | Korea | ASD: 54 HC: 38 | ASD: 79.6/20.4 HC: 47.4/52.6 | ASD: 7 HC: 6 | N/A | DSM-5 ADOS-2 ADI-R SRS IQ tests | Psychiatric evaluation IQ tests | −80 °C | No ATB 3 months and probiotic for 15 days prior sample collection | N/A | N/A |
[55] | Plaza-Díaz et al. | 2019 | Spain | ASD: 48 HC: 57 | N/A | ASD: 1.8 HC: 2.1 | ASD: 15.9 HC: 16.2 | ADOS PDD-BI ADI-R Battelle test CARS DSM-5 ICD-10 | N/A | −80 °C | No treatment of behavioural comorbidities | 24 h diet recorded Food frequency questionnaire | N/A |
[56] | Xie et al. | 2022 | China | ASD: 101 HC: 104 | ASD: 85.1/14.9 HC: 76.9/22.1 | ASD: 4.3 HC: 4.4 | ASD: 16.3 HC: 15.7 | DSM-5 CARS | N/A | −80 °C | No ATB, antifungal, AIDs, antioxidant, probiotic or prebiotic 1 month prior sample collection | Participants with special diets excluded | N/A |
[57] | Chiappori et al. | 2022 | Italy | ASD: 6 HC: 6 | ASD: 83.3/16.7 HC: 50/50 | Age range: ASD: 6–17 HC: 10–20 | N/A | DSM-5 | N/A | −80 °C | N/A | N/A | N/A |
[58] | Sun et al. | 2019 | China | ASD: 9 HC: 6 | ASD: 88.9/11.1 HC: 66.7/33.3 | Age range 3–12 | N/A | ICD-11 | N/A | −80 °C | N/A | N/A | yes |
[59] | Parracho et al. | 2005 | UK | ASD: 58 SIB: 12 HC: 10 | ASD: 82.8/17.2 SIB: 58.3/41.7 HC: 60/40 | ASD: 7 SIB: 6 HC: 6 | N/A | N/A | N/A | −20 °C | No probiotic or prebiotic in HC group for 6 months prior study, ATB usage recorded | yes | yes |
[60] | Adams et al. | 2011 | USA | ASD: 58 HC: 39 | ASD: 86.2/13.8 HC: 46.2/53.8 | ASD: 6.9 HC: 7.7 | N/A | Professional assessment ATEC | Parent report | N/A | No ATB or antifungal drugs 1 month prior sample collection, probiotic use recorded | Seafood and fish-oil consumption recorded | 6-GSI |
[61] | Wang et al. | 2011 | Australia | ASD: 23 SIB: 22 HC: 9 | ASD: 91.3/8.7 SIB: 50/50 HC: 44.4/55.6 | ASD: 5.1 SIB: 6 HC: 4.8 | N/A | CARS DSM-IV | ASSQ | −80 °C | ATB and probiotic use recorded | Special diets recorded | FGID questionnaire |
[62] | Tomova et al. | 2015 | Slovakia | ASD: 10 SIB: 9 HC: 10 | ASD: 90/10 SIB: 77.8/22.2 HC: 100/0 | Age range ASD: 2–9 SIB: 5–17 HC: 2–11 | N/A | ICD-10 CARS ADI | Psychiatric evaluation Parent interview | −80 °C | All participants medication free | N/A | Parental questionnaire |
[63] | Rose et al. | 2018 | USA | ASD: 50 HC: 41 | ASD: 84/16 HC: 92.7/7.3 | Age range 3–12 | N/A | DSM-4 ADI-R ADOS ABC | SCQ MSEL VABS ABC | N/A | No ATB or antifungal drugs 1 month prior sample collection | Dietary changes recorded | GIH Rome III |
[64] | Yitik Tonkaz et al. | 2022 | Turkey | ASD: 30 SIB: 30 HC: 30 | ASD: 86.7/11.3 SIB: 53.3/46.7 HC: 43.3/56.7 | ASD: 7.3 SIB: 9.4 HC: 8.5 | ASD: 17.7 SIB: 17.5 HC: 17.1 | Psychiatric evaluation DAWBA DSM-5 CARS | Psychiatric evaluation DAWBA | −80 °C | No ATB or antifungal drugs 2 months prior sample collection, no probiotic or prebiotic prior sample collection | Yes Participants with special diets excluded | GSI |
ADHD | |||||||||||||
[6] | Wang et al. | 2020 | Taiwan | ADHD: 30 HC: 30 | ADHD: 76.7/23.3 HC: 60/40 | ADHD: 8.4 HC: 9.3 | N/A | K-SADS-E SNAP-IV WISC ADHD-RS | K-SADS-E SNAP-IV WISC ADHD-RS | −80 °C | Patients using ATB or probiotic excluded | N/A Vegetarians excluded | N/A |
[17] | Aarts et al. | 2017 | Netherlands | ADHD: 19 HC: 77 | ADHD: 68.4/31.6 HC: 53.2/46.8 | ADHD: 19.5 HC: 27.1 | ADHD: 23.8 HC: 23.0 | DSM-4 K-SADS | N/A | −80 °C | No ATB or other medication 1 month prior sample collection | N/A | N/A |
[77] | Wan et al. | 2020 | China | ADHD: 17 HC: 17 | ADHD: 82.3/17.7 HC: 76.5/23.5 | Median age ADHD: 8 HC: 8 | ADHD: 16.1 HC: 15.9 | K-SADS CPRS | K-SADS CPRS | −80 °C | No probiotic 1 month prior sample collection N/A for ATB use | yes Participants with special diets excluded | N/A |
[78] | Jiang et al. | 2018 | China | ADHD: 51 HC: 32 | ADHD: 49/51 HC: 68/32 | ADHD: 8.5 HC: 8.5 | ADHD: 16.4 HC: 16.1 | K-SADS-PL CPRS | Clinical interview CPRS | −80 °C | No ATB and probiotic for 2 month prior sample collection or concurrent use or history of ADHD drugs | yes Vegetarians excluded | N/A |
[79] | Szopinska-Tokov et al. | 2020 | Netherlands | ADHD: 41 HC: 47 | ADHD: 63/37 Ctrl: 49/51 | ADHD: 20.2 HC: 20.5 | Median BMI ADHD: 23 HC: 22 | K-SADS CTRS CAARS | N/A | −80 °C | 19 patients using ADHD medication | N/A | N/A |
[80] | Wang et al. | 2022 | Taiwan | ADHD: 41 HC: 39 | ADHD: 73.2/26.8 HC: 56.4/43.6 | ADHD: 8 HC: 10 | ADHD: 17.5 HC: 17.8 | K-SADS-E WISC-IV Conners‘ CPT SNAP-IV | K-SADS-E | −80 °C | No AIDs, ATB or probiotic 1 month prior sample collection, no history of ADHD medication | Vegetarians excluded | N/A |
[81] | Prehn-Kristensen et al. | 2018 | Germany | ADHD: 14 HC: 17 | ADHD: 100/0 HC: 100/0 | ADHD: 11.9 HC: 13.1 | ADHD: 19.0 HC: 18.0 | K-SADS-PL CBCL FBB-HKS | K-SADS-PL CBCL FBB-HKS | Not clear | 10 patients using ADHD medication for more than 1 year, 9 of them discontinued 48h prior sample collection | yes | N/A |
Rett syndrome | |||||||||||||
[88] | Strati et al. | 2016 | Italy | RTT: 50 HC: 29 | RTT: 0/100 HC: N/A | RTT: 12 HC: 17 | N/A | Genetic testing CSS | N/A | −80 °C | No ATB, probiotic or prebiotic 3 months prior sample collection | All participants under Mediterranean-based diet | Rome III |
Anorexia Nervosa | |||||||||||||
[92] | Schulz et al. | 2020 | Germany | AN: 19 HC: 20 | AN: 0/100 HC: 0/100 | AN: 15.77 HC: 16.35 | AN: 15.8 HC: 20.3 | DSM-5 EDI BDI SCAS EDE | EDI BDI SCAS | −80 °C | No ATB or probiotic 1 month prior sample collection, other medication recorded | N/A | N/A |
Depressive Disorder | |||||||||||||
[18] | Thapa et al. | 2021 | USA | MDD: 110 HC: 27 PC: 10 | MDD: 35/65 HC: 63/37 PC: 57/43 | MDD: 19.5 HC: 20.3 PC: 19.1 | N/A | IDS, BDI-II BAI DSM-IV-TR A-LIFE | N/A | −80 °C | No ATB 6 months prior sample collection | N/A | N/A |
[94] | Ling et al. | 2022 | China | MDD: 92 HC: 48 | MDD: 45.7/54.3 HC: 45.8/54.2 | MDD: 8.84 HC: 9.27 | MDD: 21.9 HC: 21.3 | HAMD DSM-5 CCMD-3 | HAMD | −80 °C | No ATB, probiotic, prebiotic, synbiotic or psychiatric drugs 1 month prior sample collection | yes | N/A |
[95] | Zhou et al. | 2022 | China | DD: 70 HC: 101 | DD: 37.8/62.2 HC: 46.6/53.4 | D: 13.7 HC: 13.5 | D: 19.6 HC: 19.9 | ICD-10 Mini-International Neuropsych. Interview SDS SAS | Clinical interview | −80 °C | No AIDs, ATB, probiotic, prebiotic or synbiotic 1 month prior sample collection | N/A | Bristol stool scale GSRS |
Tic Disorder | |||||||||||||
[102] | Wang et al. | 2022 | China | TD: 28 HC 21 | TD: 60.7/39.3 HC: 61.9/38.1 | TD: 8.2 HC: 7.9 | TD: 19.3 HC: 18.8 | DSM-5 Expert Consensus on Diagnosis and Treatment of TD in China | No psychiatric disorder No physical illness | −80 °C | No GCs, ISs and AHs 15 days prior sample collection No ATB and probiotic 2 months prior sample collection | N/A | N/A |
[103] | Xi et al. | 2021 | China | TD: 49 HC: 50 | TD: 77.6/22.4 HC: 78/22 | TD: 8.84 HC: 8.78 | TD: 18.3 HC: matched | DSM-5 YGTSS | No psychiatric disorder | −80 °C | No ATB, probiotic, vitamins, IMs 1 month prior sample collection | N/A | GSI |
Autism + PDD − NOS | ADHD | RTT | AN | DD | TD | ||||||||||||||||||||||||||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ref. No | [59] | [35] | [60] | [61] | [47] | [42] | [31] | [48] | [62] | [49] | [50] | [36] | [25] | [51] | [63] | [52] | [26] | [37] | [27] | [28] | [43] | [55] | [58] | [29] | [38] | [53] | [30] | [39] | [40] | [44] | [19] | [32] | [54] | [41] | [57] | [45] | [64] | [33] | [46] | [34] | [56] | [17] | [78] | [81] | [79] | [77] | [6] | [80] | [88] | [92] | [18] | [94] | [95] | [103] | [102] |
Acidobacteria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Actinobacteria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Bacteroidetes | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Cyanobacteria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Firmicutes | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Fusobacteria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Proteobacteria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Verrucomicrobia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
B/F Ratio |
Autism + PDD − NOS | ADHD | RTT | AN | DD | TD | ||||||||||||||||||||||||||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ref. No | [59] | [35] | [60] | [61] | [47] | [42] | [31] | [48] | [62] | [49] | [50] | [36] | [25] | [51] | [63] | [52] | [26] | [37] | [27] | [28] | [43] | [55] | [58] | [29] | [38] | [53] | [30] | [39] | [40] | [44] | [19] | [32] | [54] | [41] | [57] | [45] | [64] | [33] | [46] | [34] | [56] | [17] | [78] | [81] | [79] | [77] | [6] | [80] | [88] | [92] | [18] | [94] | [95] | [103] | [102] |
Acetanaerobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Acetivibrio | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Acinetobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Actinomyces | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Aeromonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Agathobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Akkermansia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Alkaliflexus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Alkaliphilus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Alistipes | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Anaerofilum | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Anaerostipes | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Anaerovorax | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Bacillus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Bacteroides | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Barnesiella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Bifidobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Bilophila | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Blautia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Butyricimonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Butyrivibrio | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Citrobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Chloroplast taxa | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Chryseobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridiaceae_un | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridiales ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridium cl. I | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridium cl. IV | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridium XI | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Clostridium cl. XIVa | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Collinsella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Coprobacillus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Coprobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Coprococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Coriobacteriaceae | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Coriobacteriales_un | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Corynebacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Desulfovibrio | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Dialister | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Dorea | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Eggerthella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Eisenbergiella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Eischerichia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Eischerichia/Shigella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Enhydrobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Enterobacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Enterococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Erysipelatoclostrium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Erysipelotrichaceae | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Ethanoligenens | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Eubacterium ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Faecalibacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Flavonifractor | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Fusobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Gemmiger | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Haemophilus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Helcococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Hespellia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Klebsiella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lactobacillus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lactobacillus/Enterococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lactococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lachnobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lachnoclostridium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lachnospira | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Lachnospiraceae ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Leuconostoc | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Megamonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Megasphaera | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Mitsuokella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Neisseria | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Odoribacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Oscilospira | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Parabacteroides | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Parasutterella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Paraprevotella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Parvimonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Phascolarctobacterium | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Porphyromonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Prevotella ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Proteus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Providencia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Pseudomonas | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Pseudoramibacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Romboutsia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Roseburia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Ruminoclostridium ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Ruminococcus ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Ruminococcaceae ‡ | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Scardovia | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Shigella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Staphylococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Streptococcus | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Streptomyces | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Subdoligranulum | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Sutterella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Turicibacter | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Tyzzerella sub4 | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Veillonella | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Veillonellaceae | |||||||||||||||||||||||||||||||||||||||||||||||||||||||
Weissella |
4. Discussion and Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Cussotto, S.; Sandhu, K.V.; Dinan, T.G.; Cryan, J.F. The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective. Front. Neuroendocr. 2018, 51, 80–101. [Google Scholar] [CrossRef] [PubMed]
- Rinninella, E.; Raoul, P.; Cintoni, M.; Franceschi, F.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019, 7, 14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hemarajata, P.; Versalovic, J. Effects of probiotics on gut microbiota: Mechanisms of intestinal immunomodulation and neuromodulation. Ther. Adv. Gastroenterol. 2013, 6, 39–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blaser, M.J. Antibiotic use and its consequences for the normal microbiome. Science 2016, 352, 544–545. [Google Scholar] [CrossRef] [Green Version]
- De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J.B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad Sci. USA 2010, 107, 14691–14696. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.J.; Yang, C.Y.; Chou, W.J.; Lee, M.J.; Chou, M.C.; Kuo, H.C.; Yeh, Y.M.; Lee, S.Y.; Huang, L.H.; Li, S.C. Gut microbiota and dietary patterns in children with attention-deficit/hyperactivity disorder. Eur. Child. Adolesc. Psychiatry 2020, 29, 287–297. [Google Scholar] [CrossRef]
- Tomova, A.; Bukovsky, I.; Rembert, E.; Yonas, W.; Alwarith, J.; Barnard, N.D.; Kahleova, H. The Effects of Vegetarian and Vegan Diets on Gut Microbiota. Front. Nutr. 2019, 6, 47. [Google Scholar] [CrossRef] [Green Version]
- Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P. Human gut microbiome viewed across age and geography. Nature 2012, 486, 222–227. [Google Scholar] [CrossRef] [Green Version]
- Yatsunenko, T.; Rey, F.E.; Manary, M.J.; Trehan, I.; Dominguez-Bello, M.G.; Contreras, M.; Magris, M.; Hidalgo, G.; Baldassano, R.N.; Anokhin, A.P. From gut dysbiosis to altered brain function and mental illness: Mechanisms and pathways. Mol. Psychiatry 2016, 21, 738–748. [Google Scholar]
- Sampson, T.R.; Mazmanian, S.K. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 2015, 17, 565–576. [Google Scholar] [CrossRef] [Green Version]
- Möhle, L.; Mattei, D.; Heimesaat, M.M.; Bereswill, S.; Fischer, A.; Alutis, M.; French, T.; Hambardzumyan, D.; Matzinger, P.; Dunay, I.R.; et al. Ly6C(hi) Monocytes Provide a Link between Antibiotic-Induced Changes in Gut Microbiota and Adult Hippocampal Neurogenesis. Cell Rep. 2016, 15, 1945–1956. [Google Scholar] [CrossRef] [PubMed]
- Braniste, V.; Al-Asmakh, M.; Kowal, C.; Anuar, F.; Abbaspour, A.; Tóth, M.; Korecka, A.; Bakocevic, N.; Ng, L.G.; Kundu, P.; et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci. Transl. Med. 2014, 6, 263ra158. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dinan, T.G.; Cryan, J.F. Gut instincts: Microbiota as a key regulator of brain development, ageing and neurodegeneration. J. Physiol. 2017, 595, 489–503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Silva, Y.P.; Bernardi, A.; Frozza, R.L. The Role of Short-Chain Fatty Acids From Gut Microbiota in Gut-Brain Communication. Front. Endocrinol (Lausanne) 2020, 11, 25. [Google Scholar] [CrossRef] [Green Version]
- Boonchooduang, N.; Louthre noo, O.; Chattipakorn, N.; Chattipakorn, S.C. Possible links between gut-microbiota and attention-deficit/hyperactivity disorders in children and adolescents. Eur. J. Nutr. 2020, 59, 3391–3403. [Google Scholar] [CrossRef]
- Strandwitz, P. Neurotransmitter modulation by the gut microbiota. Brain Res. 2018, 1693, 128–133. [Google Scholar] [CrossRef]
- Aarts, E.; Ederveen, T.H.A.; Naaijen, J.; Zwiers, M.P.; Boekhorst, J.; Timmerman, H.M.; Smeekens, S.P.; Netea, M.G.; Buitelaar, J.K.; Franke, B.; et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS ONE 2017, 12, e0183509. [Google Scholar] [CrossRef] [Green Version]
- Thapa, S.; Sheu, J.C.; Venkatachalam, A.; Runge, J.K.; Luna, R.A.; Calarge, C.A. Gut microbiome in adolescent depression. J. Affect. Disord. 2021, 292, 500–507. [Google Scholar] [CrossRef]
- Cao, X.; Liu, K.; Liu, J.; Liu, Y.W.; Xu, L.; Wang, H.; Zhu, Y.; Wang, P.; Li, Z.; Wen, J.; et al. Dysbiotic Gut Microbiota and Dysregulation of Cytokine Profile in Children and Teens With Autism Spectrum Disorder. Front. Neurosci. 2021, 15, 635925. [Google Scholar] [CrossRef]
- Lord, C.; Brugha, T.S.; Charman, T.; Cusack, J.; Dumas, G.; Frazier, T.; Jones, E.J.H.; Jones, R.M.; Pickles, A.; State, M.W.; et al. Autism spectrum disorder. Nat. Rev. Dis. Primers 2020, 6, 5. [Google Scholar] [CrossRef]
- Lai, M.C.; Kassee, C.; Besney, R.; Bonato, S.; Hull, L.; Mandy, W.; Szatmari, P.; Ameis, S.H. Prevalence of co-occurring mental health diagnoses in the autism population: A systematic review and meta-analysis. Lancet Psychiatry 2019, 6, 819–829. [Google Scholar] [CrossRef]
- Sharp, W.G.; Berry, R.C.; McCracken, C.; Nuhu, N.N.; Marvel, E.; Saulnier, C.A.; Klin, A.; Jones, W.; Jaquess, D.L. Feeding problems and nutrient intake in children with autism spectrum disorders: A meta-analysis and comprehensive review of the literature. J. Autism Dev. Disord. 2013, 43, 2159–2173. [Google Scholar] [CrossRef] [PubMed]
- McElhanon, B.O.; McCracken, C.; Karpen, S.; Sharp, W.G. Gastrointestinal symptoms in autism spectrum disorder: A meta-analysis. Pediatrics 2014, 133, 872–883. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holingue, C.; Newill, C.; Lee, L.C.; Pasricha, P.J.; Daniele Fallin, M. Gastrointestinal symptoms in autism spectrum disorder: A review of the literature on ascertainment and prevalence. Autism Res. 2018, 11, 24–36. [Google Scholar] [CrossRef] [PubMed]
- 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. Differences in fecal microbial metabolites and microbiota of children with autism spectrum disorders. Anaerobe 2018, 49, 121–131. [Google Scholar] [CrossRef] [PubMed]
- Carissimi, C.; Laudadio, I.; Palone, F.; Fulci, V.; Cesi, V.; Cardona, F.; Alfonsi, C.; Cucchiara, S.; Isoldi, S.; Stronati, L. Functional analysis of gut microbiota and immunoinflammation in children with autism spectrum disorders. Dig. Liver Dis. 2019, 51, 1366–1374. [Google Scholar] [CrossRef]
- Liu, S.; Li, E.; Sun, Z.; Fu, D.; Duan, G.; Jiang, M.; Yu, Y.; Mei, L.; Yang, P.; Tang, Y.; et al. Altered gut microbiota and short chain fatty acids in Chinese children with autism spectrum disorder. Sci. Rep. 2019, 9, 287. [Google Scholar] [CrossRef] [Green Version]
- Ma, B.; Liang, J.; Dai, M.; Wang, J.; Luo, J.; Zhang, Z.; Jing, J. Altered Gut Microbiota in Chinese Children with Autism Spectrum Disorders. Front. Cell Infect. Microbiol. 2019, 9, 40. [Google Scholar] [CrossRef]
- Wang, M.; Wan, J.; Rong, H.; He, F.; Wang, H.; Zhou, J.; Cai, C.; Wang, Y.; Xu, R.; Yin, Z. Alterations in Gut Glutamate Metabolism Associated with Changes in Gut Microbiota Composition in Children with Autism Spectrum Disorder. mSystems 2019, 4, e00321-18. [Google Scholar] [CrossRef] [Green Version]
- Dan, Z.; Mao, X.; Liu, Q.; Guo, M.; Zhuang, Y.; Liu, Z.; Chen, K.; Chen, J.; Xu, R.; Tang, J. Altered gut microbial profile is associated with abnormal metabolism activity of Autism Spectrum Disorder. Gut Microbes 2020, 11, 1246–1267. [Google Scholar] [CrossRef]
- Kang, D.W.; Park, J.G.; Ilhan, Z.E.; Wallstrom, G.; Labaer, J.; Adams, J.B.; Krajmalnik-Brown, R. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS ONE 2013, 8, e68322. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Shi, K.; Liu, X.; Dai, Y.; Liu, Y.; Zhang, L.; Du, X.; Zhu, T.; Yu, J.; Fang, S.; et al. Gut Microbial Profile Is Associated with the Severity of Social Impairment and IQ Performance in Children with Autism Spectrum Disorder. Front. Psychiatry 2021, 12, 789864. [Google Scholar] [CrossRef] [PubMed]
- Vernocchi, P.; Ristori, M.V.; Guerrera, S.; Guarrasi, V.; Conte, F.; Russo, A.; Lupi, E.; Albitar-Nehme, S.; Gardini, S.; Paci, P.; et al. Gut Microbiota Ecology and Inferred Functions in Children With ASD Compared to Neurotypical Subjects. Front. Microbiol. 2022, 13, 871086. [Google Scholar] [CrossRef]
- Wong, O.W.H.; Lam, A.M.W.; Or, B.P.N.; Mo, F.Y.M.; Shea, C.K.S.; Lai, K.Y.C.; Ma, S.L.; Hung, S.F.; Chan, S.; Kwong, T.N.Y.; et al. Disentangling the relationship of gut microbiota, functional gastrointestinal disorders and autism: A case-control study on prepubertal Chinese boys. Sci. Rep. 2022, 12, 10659. [Google Scholar] [CrossRef] [PubMed]
- Finegold, S.M.; Dowd, S.E.; Gontcharova, V.; Liu, C.; Henley, K.E.; Wolcott, R.D.; Youn, E.; Summanen, P.H.; Granpeesheh, D.; Dixon, D.; et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe 2010, 16, 444–453. [Google Scholar] [CrossRef]
- Coretti, L.; Paparo, L.; Riccio, M.P.; Amato, F.; Cuomo, M.; Natale, A.; Borrelli, L.; Corrado, G.; De Caro, C.; Comegna, M.; et al. Gut Microbiota Features in Young Children with Autism Spectrum Disorders. Front. Microbiol. 2018, 9, 3146. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, N.; Yang, J.; Zhang, J.; Liang, C.; Wang, Y.; Chen, B.; Zhao, C.; Wang, J.; Zhang, G.; Zhao, D.; et al. Correlation of Gut Microbiome Between ASD Children and Mothers and Potential Biomarkers for Risk Assessment. Genom. Proteom. Bioinform. 2019, 17, 26–38. [Google Scholar] [CrossRef] [PubMed]
- Zhai, Q.; Cen, S.; Jiang, J.; Zhao, J.; Zhang, H.; Chen, W. Disturbance of trace element and gut microbiota profiles as indicators of autism spectrum disorder: A pilot study of Chinese children. Environ. Res 2019, 171, 501–509. [Google Scholar] [CrossRef]
- Ding, X.; Xu, Y.; Zhang, X.; Zhang, L.; Duan, G.; Song, C.; Li, Z.; Yang, Y.; Wang, Y.; Wang, X.; et al. Gut microbiota changes in patients with autism spectrum disorders. J. Psychiatr. Res. 2020, 129, 149–159. [Google Scholar] [CrossRef]
- Zou, R.; Xu, F.; Wang, Y.; Duan, M.; Guo, M.; Zhang, Q.; Zhao, H.; Zheng, H. Changes in the Gut Microbiota of Children with Autism Spectrum Disorder. Autism Res. 2020, 13, 1614–1625. [Google Scholar] [CrossRef]
- Ye, F.; Gao, X.; Wang, Z.; Cao, S.; Liang, G.; He, D.; Lv, Z.; Wang, L.; Xu, P.; Zhang, Q. Comparison of gut microbiota in autism spectrum disorders and neurotypical boys in China: A case-control study. Synth. Syst. Biotechnol. 2021, 6, 120–126. [Google Scholar] [CrossRef] [PubMed]
- De Angelis, M.; Piccolo, M.; Vannini, L.; Siragusa, S.; De Giacomo, A.; Serrazzanetti, D.I.; Cristofori, F.; Guerzoni, M.E.; Gobbetti, M.; Francavilla, R. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PLoS ONE 2013, 8, e76993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Niu, M.; Li, Q.; Zhang, J.; Wen, F.; Dang, W.; Duan, G.; Li, H.; Ruan, W.; Yang, P.; Guan, C.; et al. Characterization of Intestinal Microbiota and Probiotics Treatment in Children With Autism Spectrum Disorders in China. Front. Neurol. 2019, 10, 1084. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zurita, M.F.; Cárdenas, P.A.; Sandoval, M.E.; Peña, M.C.; Fornasini, M.; Flores, N.; Monaco, M.H.; Berding, K.; Donovan, S.M.; Kuntz, T.; et al. Analysis of gut microbiome, nutrition and immune status in autism spectrum disorder: A case-control study in Ecuador. Gut Microbes 2020, 11, 453–464. [Google Scholar] [CrossRef] [PubMed]
- Fujishiro, S.; Tsuji, S.; Akagawa, S.; Akagawa, Y.; Yamanouchi, S.; Ishizaki, Y.; Hashiyada, M.; Akane, A.; Kaneko, K. Dysbiosis in Gut Microbiota in Children Born Preterm Who Developed Autism Spectrum Disorder: A Pilot Study. J. Autism Dev. Disord. 2022, 1–9. [Google Scholar] [CrossRef]
- Wan, Y.; Zuo, T.; Xu, Z.; Zhang, F.; Zhan, H.; Chan, D.; Leung, T.F.; Yeoh, Y.K.; Chan, F.K.L.; Chan, R.; et al. Underdevelopment of the gut microbiota and bacteria species as non-invasive markers of prediction in children with autism spectrum disorder. Gut 2022, 71, 910–918. [Google Scholar] [CrossRef]
- Gondalia, S.V.; Palombo, E.A.; Knowles, S.R.; Cox, S.B.; Meyer, D.; Austin, D.W. Molecular characterisation of gastrointestinal microbiota of children with autism (with and without gastrointestinal dysfunction) and their neurotypical siblings. Autism Res. 2012, 5, 419–427. [Google Scholar] [CrossRef]
- Son, J.S.; Zheng, L.J.; Rowehl, L.M.; Tian, X.; Zhang, Y.; Zhu, W.; Litcher-Kelly, L.; Gadow, K.D.; Gathungu, G.; Robertson, C.E.; 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. [Google Scholar] [CrossRef]
- Strati, F.; Cavalieri, D.; Albanese, D.; De Felice, C.; Donati, C.; Hayek, J.; Jousson, O.; Leoncini, S.; Renzi, D.; Calabrò, A.; et al. New evidences on the altered gut microbiota in autism spectrum disorders. Microbiome 2017, 5, 24. [Google Scholar] [CrossRef] [Green Version]
- Berding, K.; Donovan, S.M. Diet Can Impact Microbiota Composition in Children with Autism Spectrum Disorder. Front. Neurosci. 2018, 12, 515. [Google Scholar] [CrossRef] [Green Version]
- Pulikkan, J.; Maji, A.; Dhakan, D.B.; Saxena, R.; Mohan, B.; Anto, M.M.; Agarwal, N.; Grace, T.; Sharma, V.K. Gut Microbial Dysbiosis in Indian Children with Autism Spectrum Disorders. Microb. Ecol. 2018, 76, 1102–1114. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Ma, W.; Zhang, J.; He, Y.; Wang, J. Analysis of gut microbiota profiles and microbe-disease associations in children with autism spectrum disorders in China. Sci. Rep. 2018, 8, 13981. [Google Scholar] [CrossRef] [Green Version]
- Ahmed, S.A.; Elhefnawy, A.M.; Azouz, H.G.; Roshdy, Y.S.; Ashry, M.H.; Ibrahim, A.E.; Meheissen, M.A. Study of the gut Microbiome Profile in Children with Autism Spectrum Disorder: A Single Tertiary Hospital Experience. J. Mol. Neurosci. 2020, 70, 887–896. [Google Scholar] [CrossRef] [PubMed]
- Ha, S.; Oh, D.; Lee, S.; Park, J.; Ahn, J.; Choi, S.; Cheon, K.A. Altered Gut Microbiota in Korean Children with Autism Spectrum Disorders. Nutrients 2021, 13, 3300. [Google Scholar] [CrossRef] [PubMed]
- Plaza-Díaz, J.; Gómez-Fernández, A.; Chueca, N.; Torre-Aguilar, M.J.; Gil, Á.; Perez-Navero, J.L.; Flores-Rojas, K.; Martín-Borreguero, P.; Sollis-Ura, P.; Ruiz-Ojeda, F.J.; et al. Autism Spectrum Disorder (ASD) with and without Mental Regression is Associated with Changes in the Fecal Microbiota. Nutrients 2019, 11, 337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, X.; Li, L.; Wu, X.; Hou, F.; Chen, Y.; Shi, L.; Liu, Q.; Zhu, K.; Jiang, Q.; Feng, Y.; et al. Alteration of the fecal microbiota in Chinese children with autism spectrum disorder. Autism Res. 2022, 15, 996–1007. [Google Scholar] [CrossRef]
- Chiappori, F.; Cupaioli, F.A.; Consiglio, A.; Di Nanni, N.; Mosca, E.; Licciulli, V.F.; Mezzelani, A. Analysis of Faecal Microbiota and Small ncRNAs in Autism: Detection of miRNAs and piRNAs with Possible Implications in Host-Gut Microbiota Cross-Talk. Nutrients 2022, 14, 1340. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; You, Z.; Jia, L.; Wang, F. Autism spectrum disorder is associated with gut microbiota disorder in children. BMC Pediatr. 2019, 19, 516. [Google Scholar] [CrossRef] [Green Version]
- Parracho, H.M.; Bingham, M.O.; Gibson, G.R.; McCartney, A.L. Differences between the gut microflora of children with autistic spectrum disorders and that of healthy children. J. Med. Microbiol. 2005, 54, 987–991. [Google Scholar] [CrossRef]
- Adams, J.B.; Johansen, L.J.; Powell, L.D.; Quig, D.; Rubin, R.A. Gastrointestinal flora and gastrointestinal status in children with autism--comparisons to typical children and correlation with autism severity. BMC Gastroenterol. 2011, 11, 22. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.; Christophersen, C.T.; Sorich, M.J.; Gerber, J.P.; Angley, M.T.; Conlon, M.A. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Appl. Environ. Microbiol. 2011, 77, 6718–6721. [Google Scholar] [CrossRef] [PubMed]
- Tomova, A.; Husarova, V.; Lakatosova, S.; Bakos, J.; Vlkova, B.; Babinska, K.; Ostatnikova, D. Gastrointestinal microbiota in children with autism in Slovakia. Physiol. Behav. 2015, 138, 179–187. [Google Scholar] [CrossRef] [PubMed]
- Rose, D.R.; Yang, H.; Serena, G.; Sturgeon, C.; Ma, B.; Careaga, M.; Hughes, H.K.; Angkustsiri, K.; Rose, M.; Hertz-Picciotto, I.; et al. Differential immune responses and microbiota profiles in children with autism spectrum disorders and co-morbid gastrointestinal symptoms. Brain Behav. Immun. 2018, 70, 354–368. [Google Scholar] [CrossRef] [PubMed]
- Yitik Tonkaz, G.; Esin, I.S.; Turan, B.; Uslu, H.; Dursun, O.B. Determinants of Leaky Gut and Gut Microbiota Differences in Children with Autism Spectrum Disorder and Their Siblings. J. Autism Dev. Disord. 2022, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Tomova, A.; Soltys, K.; Kemenyova, P.; Karhanek, M.; Babinska, K. The Influence of Food Intake Specificity in Children with Autism on Gut Microbiota. Int. J. Mol. Sci. 2020, 21, 2797. [Google Scholar] [CrossRef] [Green Version]
- Siniscalco, D.; Schultz, S.; Brigida, A.L.; Antonucci, N. Inflammation and Neuro-Immune Dysregulations in Autism Spectrum Disorders. Pharmaceuticals 2018, 11, 56. [Google Scholar] [CrossRef] [Green Version]
- Pellegrini, L.; Foglio, E.; Pontemezzo, E.; Germani, A.; Russo, M.A.; Limana, F. HMGB1 and repair: Focus on the heart. Pharmacol. Ther. 2019, 196, 160–182. [Google Scholar] [CrossRef]
- Chen, R.; Kang, R.; Tang, D. The mechanism of HMGB1 secretion and release. Exp. Mol. Med. 2022, 54, 91–102. [Google Scholar] [CrossRef]
- Babinská, K.; Tomova, A.; Celušáková, H.; Babková, J.; Repiská, G.; Kubranská, A.; Filčíková, D.; Siklenková, L.; Ostatníková, D. Fecal calprotectin levels correlate with main domains of the autism diagnostic interview-revised (ADI-R) in a sample of individuals with autism spectrum disorders from Slovakia. Physiol. Res. 2017, 66, S517–S522. [Google Scholar] [CrossRef]
- de Theije, C.G.; Wu, J.; da Silva, S.L.; Kamphuis, P.J.; Garssen, J.; Korte, S.M.; Kraneveld, A.D. Pathways underlying the gut-to-brain connection in autism spectrum disorders as future targets for disease management. Eur. J. Pharm. 2011, 668, S70–S80. [Google Scholar] [CrossRef]
- Louis, P.; Flint, H.J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 2017, 19, 29–41. [Google Scholar] [CrossRef] [PubMed]
- Parada Venegas, D.; De la Fuente, M.K.; Landskron, G.; González, M.J.; Quera, R.; Dijkstra, G.; Harmsen, H.J.M.; Faber, K.N.; Hermoso, M.A. Short Chain Fatty Acids (SCFAs)-Mediated Gut Epithelial and Immune Regulation and Its Relevance for Inflammatory Bowel Diseases. Front. Immunol 2019, 10, 277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Frye, R.E.; Rose, S.; Chacko, J.; Wynne, R.; Bennuri, S.C.; Slattery, J.C.; Tippett, M.; Delhey, L.; Melnyk, S.; Kahler, S.G.; et al. Modulation of mitochondrial function by the microbiome metabolite propionic acid in autism and control cell lines. Transl. Psychiatry 2016, 6, e927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nafday, S.M.; Chen, W.; Peng, L.; Babyatsky, M.W.; Holzman, I.R.; Lin, J. Short-chain fatty acids induce colonic mucosal injury in rats with various postnatal ages. Pediatr. Res. 2005, 57, 201–204. [Google Scholar] [CrossRef] [Green Version]
- Thomas, R.; Sanders, S.; Doust, J.; Beller, E.; Glasziou, P. Prevalence of attention-deficit/hyperactivity disorder: A systematic review and meta-analysis. Pediatrics 2015, 135, e994–e1001. [Google Scholar] [CrossRef] [Green Version]
- Drechsler, R.; Brem, S.; Brandeis, D.; Grünblatt, E.; Berger, G.; Walitza, S. ADHD: Current Concepts and Treatments in Children and Adolescents. Neuropediatrics 2020, 51, 315–335. [Google Scholar] [CrossRef]
- Wan, L.; Ge, W.R.; Zhang, S.; Sun, Y.L.; Wang, B.; Yang, G. Case-Control Study of the Effects of Gut Microbiota Composition on Neurotransmitter Metabolic Pathways in Children with Attention Deficit Hyperactivity Disorder. Front. Neurosci. 2020, 14, 127. [Google Scholar] [CrossRef] [Green Version]
- Jiang, H.Y.; Zhou, Y.Y.; Zhou, G.L.; Li, Y.C.; Yuan, J.; Li, X.H.; Ruan, B. Gut microbiota profiles in treatment-naïve children with attention deficit hyperactivity disorder. Behav. Brain Res. 2018, 347, 408–413. [Google Scholar] [CrossRef]
- Szopinska-Tokov, J.; Dam, S.; Naaijen, J.; Konstanti, P.; Rommelse, N.; Belzer, C.; Buitelaar, J.; Franke, B.; Bloemendaal, M.; Aarts, E.; et al. Investigating the Gut Microbiota Composition of Individuals with Attention-Deficit/Hyperactivity Disorder and Association with Symptoms. Microorganisms 2020, 8, 406. [Google Scholar] [CrossRef] [Green Version]
- Wang, L.J.; Li, S.C.; Li, S.W.; Kuo, H.C.; Lee, S.Y.; Huang, L.H.; Chin, C.Y.; Yang, C.Y. Gut microbiota and plasma cytokine levels in patients with attention-deficit/hyperactivity disorder. Transl. Psychiatry 2022, 12, 76. [Google Scholar] [CrossRef]
- Prehn-Kristensen, A.; Zimmermann, A.; Tittmann, L.; Lieb, W.; Schreiber, S.; Baving, L.; Fisher, A. Reduced microbiome alpha diversity in young patients with ADHD. PLoS ONE 2018, 13, e0200728. [Google Scholar]
- Šoltýsová, M.; Tomova, A.; Ostatníková, D. Vzájomný vzťah medzi črevnou mikrobiotou a vybranými psychofarmakami. Česká A Slov. Psychiatr. 2021, 117, 577–583. [Google Scholar]
- Quagliariello, A.; Del Chierico, F.; Russo, A.; Reddel, S.; Conte, G.; Lopetuso, L.R.; Ianiro, G.; Dallapiccola, B.; Cardona, F.; Gasbarrini, A.; et al. Gut Microbiota Profiling and Gut-Brain Crosstalk in Children Affected by Pediatric Acute-Onset Neuropsychiatric Syndrome and Pediatric Autoimmune Neuropsychiatric Disorders Associated With Streptococcal Infections. Front. Microbiol. 2018, 9, 675. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maini Rekdal, V.; Bess, E.N.; Bisanz, J.E.; Turnbaugh, P.J.; Balskus, E.P. Discovery and inhibition of an interspecies gut bacterial pathway for Levodopa metabolism. Science 2019, 364, eaau6323. [Google Scholar] [CrossRef] [Green Version]
- Amir, R.E.; Van den Veyver, I.B.; Schultz, R.; Malicki, D.M.; Tran, C.Q.; Dahle, E.J.; Philippi, A.; Timar, L.; Percy, A.K.; Motil, K.J.; et al. Influence of mutation type and X chromosome inactivation on Rett syndrome phenotypes. Ann. Neurol. 2000, 47, 670–679. [Google Scholar] [CrossRef]
- Smeets, E.E.; Pelc, K.; Dan, B. Rett Syndrome. Mol. Syndr. 2012, 2, 113–127. [Google Scholar] [CrossRef]
- Motil, K.J.; Caeg, E.; Barrish, J.O.; Geerts, S.; Lane, J.B.; Percy, A.K.; Annese, F.; McNair, L.; Skinner, S.A.; Lee, H.S.; et al. Gastrointestinal and nutritional problems occur frequently throughout life in girls and women with Rett syndrome. J. Pediatr. Gastroenterol. Nutr. 2012, 55, 292–298. [Google Scholar] [CrossRef] [Green Version]
- Strati, F.; Cavalieri, D.; Albanese, D.; De Felice, C.; Donati, C.; Hayek, J.; Jousson, O.; Leoncini, S.; Pindo, M.; Renzi, D.; et al. Altered gut microbiota in Rett syndrome. Microbiome 2016, 4, 41. [Google Scholar] [CrossRef] [Green Version]
- Keski-Rahkonen, A.; Mustelin, L. Epidemiology of eating disorders in Europe: Prevalence, incidence, comorbidity, course, consequences, and risk factors. Curr. Opin. Psychiatry 2016, 29, 340–345. [Google Scholar] [CrossRef]
- Smink, F.R.; van Hoeken, D.; Hoek, H.W. Epidemiology of eating disorders: Incidence, prevalence and mortality rates. Curr. Psychiatry Rep. 2012, 14, 406–414. [Google Scholar] [CrossRef] [Green Version]
- Herpertz-Dahlmann, B.; Dahmen, B. Children in Need-Diagnostics, Epidemiology, Treatment and Outcome of Early Onset Anorexia Nervosa. Nutrients 2019, 11, 1932. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schulz, N.; Belheouane, M.; Dahmen, B.; Ruan, V.A.; Specht, H.E.; Dempfle, A.; Herpetz-Dahlmann, B.; Baines, J.F.; Seitz, J. Gut microbiota alteration in adolescent anorexia nervosa does not normalize with short-term weight restoration. Int. J. Eat. Disord. 2021, 54, 969–980. [Google Scholar] [CrossRef] [PubMed]
- Avenevoli, S.; Swendsen, J.; He, J.P.; Burstein, M.; Merikangas, K.R. Major depression in the national comorbidity survey-adolescent supplement: Prevalence, correlates, and treatment. J. Am. Acad. Child Adolesc. Psychiatry 2015, 54, 37–44.e2. [Google Scholar] [CrossRef] [PubMed]
- Ling, Z.; Cheng, Y.; Chen, F.; Yan, X.; Liu, X.; Shao, L.; Jin, G.; Zhou, D.; Jiang, G.; Li, H.; et al. Changes in fecal microbiota composition and the cytokine expression profile in school-aged children with depression: A case-control study. Front. Immunol. 2022, 13, 964910. [Google Scholar] [CrossRef]
- Zhou, Y.Y.; Zhang, X.; Pan, L.Y.; Zhang, W.W.; Chen, F.; Hu, S.S.; Jiang, H.Y. Fecal microbiota in pediatric depression and its relation to bowel habits. J. Psychiatr. Res. 2022, 150, 113–121. [Google Scholar] [CrossRef]
- Rhee, S.J.; Kim, H.; Lee, Y.; Lee, H.J.; Park, C.H.K.; Yang, J.; Kim, Y.K.; Ahn, Y.M. The association between serum microbial DNA composition and symptoms of depression and anxiety in mood disorders. Sci. Rep. 2021, 11, 13987. [Google Scholar] [CrossRef]
- Jiang, H.; Ling, Z.; Zhang, Y.; Mao, H.; Ma, Z.; Yin, Y.; Wang, W.; Tang, W.; Tan, Z.; Shi, J.; et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav. Immun. 2015, 48, 186–194. [Google Scholar] [CrossRef] [Green Version]
- Michels, N.; Van de Wiele, T.; Fouhy, F.; O’Mahony, S.; Clarke, G.; Keane, J. Gut microbiome patterns depending on children’s psychosocial stress: Reports versus biomarkers. Brain Behav. Immun. 2019, 80, 751–762. [Google Scholar] [CrossRef]
- Wanderer, S.; Roessner, V.; Freeman, R.; Bock, N.; Rothenberger, A.; Becker, A. Relationship of obsessive-compulsive disorder to age-related comorbidity in children and adolescents with Tourette syndrome. J. Dev. Behav. Pediatr. 2012, 33, 124–133. [Google Scholar] [CrossRef]
- Roessner, V.; Schoenefeld, K.; Buse, J.; Bender, S.; Ehrlich, S.; Münchau, A. Pharmacological treatment of tic disorders and Tourette Syndrome. Neuropharmacology 2013, 68, 143–149. [Google Scholar] [CrossRef]
- Hoekstra, P.J.; Dietrich, A.; Edwards, M.J.; Elamin, I.; Martino, D. Environmental factors in Tourette syndrome. Neurosci. Biobehav. Rev. 2013, 37, 1040–1049. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Xu, H.; Jing, M.; Hu, X.; Wang, J.; Hua, Y. Gut Microbiome Composition Abnormalities Determined Using High-Throughput Sequencing in Children with Tic Disorder. Front. Pediatr. 2022, 10, 831944. [Google Scholar] [CrossRef] [PubMed]
- Xi, W.; Gao, X.; Zhao, H.; Luo, X.; Li, J.; Tan, X.; Wang, L.; Zhao, J.B.; Wang, J.; Yang, G.; et al. Depicting the composition of gut microbiota in children with tic disorders: An exploratory study. J. Child. Psychol. Psychiatry 2021, 62, 1246–1254. [Google Scholar] [CrossRef] [PubMed]
- Bernard, N.J. Rheumatoid arthritis: Prevotella copri associated with new-onset untreated RA. Nat. Rev. Rheumatol. 2014, 10, 2. [Google Scholar] [CrossRef] [PubMed]
- Yeon, S.M.; Lee, J.H.; Kang, D.; Bae, H.; Lee, K.Y.; Jin, S.; Kim, J.R.; Jung, Y.W.; Park, T.W. A cytokine study of pediatric Tourette’s disorder without obsessive compulsive disorder. Psychiatry Res. 2017, 247, 90–96. [Google Scholar] [CrossRef]
- Mariat, D.; Firmesse, O.; Levenez, F.; Guimarăes, V.; Sokol, H.; Doré, J.; Corthier, G.; Furet, J.P. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 2009, 9, 123. [Google Scholar] [CrossRef]
- Knudsen, J.K.; Bundgaard-Nielsen, C.; Hjerrild, S.; Nielsen, R.E.; Leutscher, P.; Sørensen, S. Gut microbiota variations in patients diagnosed with major depressive disorder-A systematic review. Brain Behav. 2021, 11, e02177. [Google Scholar] [CrossRef]
- Zhao, H.; Jin, K.; Jiang, C.; Pan, F.; Wu, J.; Luan, H.; Zhao, Z.; Chen, J.; Mou, T.; Wang, Z.; et al. A pilot exploration of multi-omics research of gut microbiome in major depressive disorders. Transl. Psychiatry 2022, 12, 8. [Google Scholar] [CrossRef]
- McGuinness, A.J.; Davis, J.A.; Dawson, S.L.; Loughman, A.; Collier, F.; O’Hely, M.; Simpson, C.A.; Green, J.; Marx, W.; Hair, C.; et al. A systematic review of gut microbiota composition in observational studies of major depressive disorder, bipolar disorder and schizophrenia. Mol. Psychiatry 2022, 27, 1920–1935. [Google Scholar] [CrossRef]
- Zhang, Q.; Zou, R.; Guo, M.; Duan, M.; Li, Q.; Zheng, H. Comparison of gut microbiota between adults with autism spectrum disorder and obese adults. PeerJ 2021, 9, e10946. [Google Scholar] [CrossRef]
- Gonzales, J.; Marchix, J.; Aymeric, L.; Le Berre-Scoul, C.; Zoppi, J.; Bordron, P.; Burel, M.; Davidovic, L.; Richard, J.R.; Gaman, A.; et al. Fecal Supernatant from Adult with Autism Spectrum Disorder Alters Digestive Functions, Intestinal Epithelial Barrier, and Enteric Nervous System. Microorganisms 2021, 9, 1723. [Google Scholar] [CrossRef] [PubMed]
- Alamoudi, M.U.; Hosie, S.; Shindler, A.E.; Wood, J.L.; Franks, A.E.; Hill-Yardin, E.L. Comparing the Gut Microbiome in Autism and Preclinical Models: A Systematic Review. Front. Cell Infect. Microbiol. 2022, 12, 905841. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Soltysova, M.; Tomova, A.; Ostatnikova, D. Gut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders. Microorganisms 2022, 10, 2009. https://doi.org/10.3390/microorganisms10102009
Soltysova M, Tomova A, Ostatnikova D. Gut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders. Microorganisms. 2022; 10(10):2009. https://doi.org/10.3390/microorganisms10102009
Chicago/Turabian StyleSoltysova, Marcela, Aleksandra Tomova, and Daniela Ostatnikova. 2022. "Gut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders" Microorganisms 10, no. 10: 2009. https://doi.org/10.3390/microorganisms10102009
APA StyleSoltysova, M., Tomova, A., & Ostatnikova, D. (2022). Gut Microbiota Profiles in Children and Adolescents with Psychiatric Disorders. Microorganisms, 10(10), 2009. https://doi.org/10.3390/microorganisms10102009