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Erschienen in: World Journal of Pediatrics 1/2021

12.06.2020 | Review Article

Intestinal microbiota and juvenile idiopathic arthritis: current understanding and future prospective

verfasst von: Le Xin, Feng He, Sen Li, Zhi-Xuan Zhou, Xiao-Lin Ma

Erschienen in: World Journal of Pediatrics | Ausgabe 1/2021

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Abstract

Background

Juvenile idiopathic arthritis (JIA) characterized by arthritis of unknown origin is the most common childhood chronic rheumatic disease, caused by both host genetic factors and environmental triggers. Recent evidence has mounted to focus on the intestinal microbiota, a potentially recognized set of environmental triggers affecting JIA development. Here we offer an overview of recently published animal and human studies that support the impact of intestinal microbiota in JIA.

Data sources

We searched PubMed for animal and human studies publications with the search terms “intestinal microbiota or gut microbiota” and “juvenile idiopathic arthritis or juvenile chronic arthritis or juvenile rheumatoid arthritis or childhood rheumatoid arthritis or pediatric rheumatoid arthritis”.

Results

Several comparative studies have demonstrated that intestinal microbial alterations might be triggers in disease pathogenesis. Alternatively, a slice of studies has suggested environmental triggers in early life might disrupt intestinal microbial colonization, including cesarean section, formula feeding, and antibiotic exposure. Aberrant intestinal microbiota may influence the development of JIA by mediating host immune programming and by altering mucosal permeability.

Conclusions

Specific microbial factors may contribute to the pathogenesis of JIA. Intensive studies, however, are warranted to investigate the causality between intestinal dysbiosis and JIA and the mechanisms behind these epidemiologic relationships. Studies are also needed to design the best interventional administrations to restore balanced intestinal microbial communities.
Literatur
1.
Zurück zum Zitat Prakken B, Albani S, Martini A. Juvenile idiopathic arthritis. Lancet. 2011;377:2138–49.PubMed Prakken B, Albani S, Martini A. Juvenile idiopathic arthritis. Lancet. 2011;377:2138–49.PubMed
2.
Zurück zum Zitat Pardeo M, Bracaglia C, De Benedetti F. Systemic juvenile idiopathic arthritis: new insights into pathogenesis and cytokine directed therapies. Best Pract Res Clin Rheumatol. 2017;31:505–16.PubMed Pardeo M, Bracaglia C, De Benedetti F. Systemic juvenile idiopathic arthritis: new insights into pathogenesis and cytokine directed therapies. Best Pract Res Clin Rheumatol. 2017;31:505–16.PubMed
3.
Zurück zum Zitat Nistala K, Moncrieffe H, Newton KR, Varsani H, Hunter P, Wedderburn LR. Interleukin-17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum. 2008;58:875–87.PubMedPubMedCentral Nistala K, Moncrieffe H, Newton KR, Varsani H, Hunter P, Wedderburn LR. Interleukin-17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum. 2008;58:875–87.PubMedPubMedCentral
4.
Zurück zum Zitat Hori S, Takahashi T, Sakaguchi S. Control of autoimmunity by naturally arising regulatory CD4+ T cells. Adv Immunol. 2003;81:331–71.PubMed Hori S, Takahashi T, Sakaguchi S. Control of autoimmunity by naturally arising regulatory CD4+ T cells. Adv Immunol. 2003;81:331–71.PubMed
5.
Zurück zum Zitat Hu Z, Jiang K, Frank MB, Chen Y, Jarvis JN. Complexity and specificity of the neutrophil transcriptomes in juvenile idiopathic arthritis. Sci Rep. 2016;6:27453.PubMedPubMedCentral Hu Z, Jiang K, Frank MB, Chen Y, Jarvis JN. Complexity and specificity of the neutrophil transcriptomes in juvenile idiopathic arthritis. Sci Rep. 2016;6:27453.PubMedPubMedCentral
6.
Zurück zum Zitat Jiang K, Frank M, Chen Y, Osban J, Jarvis JN. Genomic characterization of remission in juvenile idiopathic arthritis. Arthritis Res Ther. 2013;15:R100.PubMedPubMedCentral Jiang K, Frank M, Chen Y, Osban J, Jarvis JN. Genomic characterization of remission in juvenile idiopathic arthritis. Arthritis Res Ther. 2013;15:R100.PubMedPubMedCentral
7.
Zurück zum Zitat Roche-Lima A, Carrasquillo-Carrion K, Gomez-Moreno R, Cruz JM, Velazquez-Morales DM, Rogozin IB, et al. The presence of genotoxic and/or pro-inflammatory bacterial genes in gut metagenomic databases and their possible link with inflammatory bowel diseases. Front Genet. 2018;9:116.PubMedPubMedCentral Roche-Lima A, Carrasquillo-Carrion K, Gomez-Moreno R, Cruz JM, Velazquez-Morales DM, Rogozin IB, et al. The presence of genotoxic and/or pro-inflammatory bacterial genes in gut metagenomic databases and their possible link with inflammatory bowel diseases. Front Genet. 2018;9:116.PubMedPubMedCentral
8.
Zurück zum Zitat Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895–905.PubMed Zhang X, Zhang D, Jia H, Feng Q, Wang D, Liang D, et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat Med. 2015;21:895–905.PubMed
9.
Zurück zum Zitat Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell. 1996;87:811–22.PubMed Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell. 1996;87:811–22.PubMed
10.
Zurück zum Zitat Horai R, Saijo S, Tanioka H, Nakae S, Sudo K, Okahara A, et al. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J Exp Med. 2000;191:313–20.PubMedPubMedCentral Horai R, Saijo S, Tanioka H, Nakae S, Sudo K, Okahara A, et al. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J Exp Med. 2000;191:313–20.PubMedPubMedCentral
11.
Zurück zum Zitat Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature. 2003;426:454–60.PubMed Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature. 2003;426:454–60.PubMed
12.
Zurück zum Zitat Abdollahi-Roodsaz S, Joosten LA, Koenders MI, Devesa I, Roelofs MF, Radstake TR, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Investig. 2008;118:205–16.PubMed Abdollahi-Roodsaz S, Joosten LA, Koenders MI, Devesa I, Roelofs MF, Radstake TR, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Investig. 2008;118:205–16.PubMed
13.
Zurück zum Zitat Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, et al. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity. 1999;10:451–61.PubMed Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, et al. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity. 1999;10:451–61.PubMed
14.
Zurück zum Zitat Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32:815–27.PubMedPubMedCentral Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010;32:815–27.PubMedPubMedCentral
15.
Zurück zum Zitat Asquith MJ, Stauffer P, Davin S, Mitchell C, Lin P, Rosenbaum JT. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 2016;68:2151–62.PubMedPubMedCentral Asquith MJ, Stauffer P, Davin S, Mitchell C, Lin P, Rosenbaum JT. Perturbed mucosal immunity and dysbiosis accompany clinical disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 2016;68:2151–62.PubMedPubMedCentral
16.
Zurück zum Zitat Lin P, Bach M, Asquith M, Lee AY, Akileswaran L, Stauffer P, et al. HLA-B27 and human beta2-microglobulin affect the gut microbiota of transgenic rats. PLoS One. 2014;9:e105684.PubMedPubMedCentral Lin P, Bach M, Asquith M, Lee AY, Akileswaran L, Stauffer P, et al. HLA-B27 and human beta2-microglobulin affect the gut microbiota of transgenic rats. PLoS One. 2014;9:e105684.PubMedPubMedCentral
17.
Zurück zum Zitat Asquith M, Davin S, Stauffer P, Michell C, Janowitz C, Lin P, et al. Intestinal metabolites are profoundly altered in the context of HLA-B27 expression and functionally modulate disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 2017;69:1984–95.PubMedPubMedCentral Asquith M, Davin S, Stauffer P, Michell C, Janowitz C, Lin P, et al. Intestinal metabolites are profoundly altered in the context of HLA-B27 expression and functionally modulate disease in a rat model of spondyloarthritis. Arthritis Rheumatol. 2017;69:1984–95.PubMedPubMedCentral
18.
Zurück zum Zitat Maeda Y, Kurakawa T, Umemoto E, Motooka D, Ito Y, Gotoh K, et al. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol. 2016;68:2646–61.PubMed Maeda Y, Kurakawa T, Umemoto E, Motooka D, Ito Y, Gotoh K, et al. Dysbiosis contributes to arthritis development via activation of autoreactive T cells in the intestine. Arthritis Rheumatol. 2016;68:2646–61.PubMed
19.
Zurück zum Zitat Stoll ML, Kumar R, Morrow CD, Lefkowitz EJ, Cui X, Genin A, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther. 2014;16:486.PubMedPubMedCentral Stoll ML, Kumar R, Morrow CD, Lefkowitz EJ, Cui X, Genin A, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther. 2014;16:486.PubMedPubMedCentral
20.
Zurück zum Zitat Tejesvi MV, Arvonen M, Kangas SM, Keskitalo PL, Pirttila AM, Karttunen TJ, et al. Faecal microbiome in new-onset juvenile idiopathic arthritis. Eur J Clin Microbiol Infect Dis. 2016;35:363–70.PubMed Tejesvi MV, Arvonen M, Kangas SM, Keskitalo PL, Pirttila AM, Karttunen TJ, et al. Faecal microbiome in new-onset juvenile idiopathic arthritis. Eur J Clin Microbiol Infect Dis. 2016;35:363–70.PubMed
21.
Zurück zum Zitat Di Paola M, Cavalieri D, Albanese D, Sordo M, Pindo M, Donati C, et al. Alteration of fecal microbiota profiles in juvenile idiopathic arthritis. Associations with HLA-B27 allele and disease status. Front Microbiol. 2016;7:1703.PubMedPubMedCentral Di Paola M, Cavalieri D, Albanese D, Sordo M, Pindo M, Donati C, et al. Alteration of fecal microbiota profiles in juvenile idiopathic arthritis. Associations with HLA-B27 allele and disease status. Front Microbiol. 2016;7:1703.PubMedPubMedCentral
22.
Zurück zum Zitat Hissink Muller P, de Meij TGJ, Westedt M, de Groot EFJ, Allaart CF, Brinkman DMC, et al. Disturbance of microbial core species in new-onset juvenile idiopathic arthritis. J Pediatr Infect Dis. 2017;12:131–5. Hissink Muller P, de Meij TGJ, Westedt M, de Groot EFJ, Allaart CF, Brinkman DMC, et al. Disturbance of microbial core species in new-onset juvenile idiopathic arthritis. J Pediatr Infect Dis. 2017;12:131–5.
23.
Zurück zum Zitat Aggarwal A, Sarangi AN, Gaur P, Shukla A, Aggarwal R. Gut microbiome in children with enthesitis-related arthritis in a developing country and the effect of probiotic administration. Clin Exp Immunol. 2017;187:480–9.PubMed Aggarwal A, Sarangi AN, Gaur P, Shukla A, Aggarwal R. Gut microbiome in children with enthesitis-related arthritis in a developing country and the effect of probiotic administration. Clin Exp Immunol. 2017;187:480–9.PubMed
24.
Zurück zum Zitat Stoll ML, Weiss PF, Weiss JE, Nigrovic PA, Edelheit BS, Bridges SL Jr, et al. Age and fecal microbial strain-specific differences in patients with spondyloarthritis. Arthritis Res Ther. 2018;20:14.PubMedPubMedCentral Stoll ML, Weiss PF, Weiss JE, Nigrovic PA, Edelheit BS, Bridges SL Jr, et al. Age and fecal microbial strain-specific differences in patients with spondyloarthritis. Arthritis Res Ther. 2018;20:14.PubMedPubMedCentral
25.
Zurück zum Zitat van Dijkhuizen EHP, Del Chierico F, Malattia C, Russo A, Pires Marafon D, Ter Haar NM, et al. Microbiome analytics of the gut microbiota in patients with juvenile idiopathic arthritis: a longitudinal observational cohort study. Arthritis Rheumatol. 2019;71:1000–10.PubMedPubMedCentral van Dijkhuizen EHP, Del Chierico F, Malattia C, Russo A, Pires Marafon D, Ter Haar NM, et al. Microbiome analytics of the gut microbiota in patients with juvenile idiopathic arthritis: a longitudinal observational cohort study. Arthritis Rheumatol. 2019;71:1000–10.PubMedPubMedCentral
26.
Zurück zum Zitat Berntson L, Agback P, Dicksved J. Changes in fecal microbiota and metabolomics in a child with juvenile idiopathic arthritis (JIA) responding to two treatment periods with exclusive enteral nutrition (EEN). Clin Rheumatol. 2016;35:1501–6.PubMed Berntson L, Agback P, Dicksved J. Changes in fecal microbiota and metabolomics in a child with juvenile idiopathic arthritis (JIA) responding to two treatment periods with exclusive enteral nutrition (EEN). Clin Rheumatol. 2016;35:1501–6.PubMed
27.
Zurück zum Zitat Kolho KL, Korpela K, Jaakkola T, Pichai MV, Zoetendal EG, Salonen A, et al. Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am J Gastroenterol. 2015;110:921–30.PubMed Kolho KL, Korpela K, Jaakkola T, Pichai MV, Zoetendal EG, Salonen A, et al. Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am J Gastroenterol. 2015;110:921–30.PubMed
28.
Zurück zum Zitat Reyman M, van Houten MA, van Baarle D, Bosch A, Man WH, Chu M, et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;10:4997.PubMedPubMedCentral Reyman M, van Houten MA, van Baarle D, Bosch A, Man WH, Chu M, et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;10:4997.PubMedPubMedCentral
29.
Zurück zum Zitat Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T, et al. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS One. 2013;8:e78331.PubMedPubMedCentral Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T, et al. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS One. 2013;8:e78331.PubMedPubMedCentral
30.
Zurück zum Zitat Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–21.PubMed Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–21.PubMed
31.
Zurück zum Zitat Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559–66.PubMed Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by caesarean section. Gut. 2014;63:559–66.PubMed
32.
Zurück zum Zitat Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8:343ra82.PubMedPubMedCentral Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8:343ra82.PubMedPubMedCentral
33.
Zurück zum Zitat Carlens C, Jacobsson L, Brandt L, Cnattingius S, Stephansson O, Askling J. Perinatal characteristics, early life infections and later risk of rheumatoid arthritis and juvenile idiopathic arthritis. Ann Rheum Dis. 2009;68:1159–64.PubMed Carlens C, Jacobsson L, Brandt L, Cnattingius S, Stephansson O, Askling J. Perinatal characteristics, early life infections and later risk of rheumatoid arthritis and juvenile idiopathic arthritis. Ann Rheum Dis. 2009;68:1159–64.PubMed
34.
Zurück zum Zitat Kristensen K, Henriksen L. Cesarean section and disease associated with immune function. J Allergy Clin Immunol. 2016;137:587–90.PubMed Kristensen K, Henriksen L. Cesarean section and disease associated with immune function. J Allergy Clin Immunol. 2016;137:587–90.PubMed
35.
Zurück zum Zitat Sevelsted A, Stokholm J, Bonnelykke K, Bisgaard H. Cesarean section and chronic immune disorders. Pediatrics. 2015;135:e92–8.PubMed Sevelsted A, Stokholm J, Bonnelykke K, Bisgaard H. Cesarean section and chronic immune disorders. Pediatrics. 2015;135:e92–8.PubMed
36.
Zurück zum Zitat Mason T, Rabinovich CE, Fredrickson DD, Amoroso K, Reed AM, Stein LD, et al. Breast feeding and the development of juvenile rheumatoid arthritis. J Rheumatol. 1995;22:1166–70.PubMed Mason T, Rabinovich CE, Fredrickson DD, Amoroso K, Reed AM, Stein LD, et al. Breast feeding and the development of juvenile rheumatoid arthritis. J Rheumatol. 1995;22:1166–70.PubMed
37.
Zurück zum Zitat Rosenberg AM. Evaluation of associations between breast feeding and subsequent development of juvenile rheumatoid arthritis. J Rheumatol. 1996;23:1080–2.PubMed Rosenberg AM. Evaluation of associations between breast feeding and subsequent development of juvenile rheumatoid arthritis. J Rheumatol. 1996;23:1080–2.PubMed
38.
Zurück zum Zitat Hyrich KL, Baildam E, Pickford H, Chieng A, Davidson JE, Foster H, et al. Influence of past breast feeding on pattern and severity of presentation of juvenile idiopathic arthritis. Arch Dis Child. 2016;101:348–51.PubMed Hyrich KL, Baildam E, Pickford H, Chieng A, Davidson JE, Foster H, et al. Influence of past breast feeding on pattern and severity of presentation of juvenile idiopathic arthritis. Arch Dis Child. 2016;101:348–51.PubMed
39.
Zurück zum Zitat Kindgren E, Fredrikson M, Ludvigsson J. Early feeding and risk of juvenile idiopathic arthritis: a case control study in a prospective birth cohort. Pediatr Rheumatol Online J. 2017;15:46.PubMedPubMedCentral Kindgren E, Fredrikson M, Ludvigsson J. Early feeding and risk of juvenile idiopathic arthritis: a case control study in a prospective birth cohort. Pediatr Rheumatol Online J. 2017;15:46.PubMedPubMedCentral
40.
Zurück zum Zitat Arvonen M, Virta LJ, Pokka T, Kroger L, Vahasalo P. Repeated exposure to antibiotics in infancy: a predisposing factor for juvenile idiopathic arthritis or a sign of this group's greater susceptibility to infections? J Rheumatol. 2015;42:521–6.PubMed Arvonen M, Virta LJ, Pokka T, Kroger L, Vahasalo P. Repeated exposure to antibiotics in infancy: a predisposing factor for juvenile idiopathic arthritis or a sign of this group's greater susceptibility to infections? J Rheumatol. 2015;42:521–6.PubMed
41.
Zurück zum Zitat Arvonen M, Berntson L, Pokka T, Karttunen TJ, Vahasalo P, Stoll ML. Gut microbiota-host interactions and juvenile idiopathic arthritis. Pediatr Rheumatol Online J. 2016;14:44.PubMedPubMedCentral Arvonen M, Berntson L, Pokka T, Karttunen TJ, Vahasalo P, Stoll ML. Gut microbiota-host interactions and juvenile idiopathic arthritis. Pediatr Rheumatol Online J. 2016;14:44.PubMedPubMedCentral
42.
Zurück zum Zitat Horton DB, Scott FI, Haynes K, Putt ME, Rose CD, Lewis JD, et al. Antibiotic exposure and juvenile idiopathic arthritis: a case-control study. Pediatrics. 2015;136:e333–43.PubMedPubMedCentral Horton DB, Scott FI, Haynes K, Putt ME, Rose CD, Lewis JD, et al. Antibiotic exposure and juvenile idiopathic arthritis: a case-control study. Pediatrics. 2015;136:e333–43.PubMedPubMedCentral
43.
Zurück zum Zitat Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23:314–26.PubMedPubMedCentral Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23:314–26.PubMedPubMedCentral
44.
Zurück zum Zitat Ardeshir A, Narayan NR, Mendez-Lagares G, Lu D, Rauch M, Huang Y, et al. Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems. Sci Transl Med. 2014;6:252ra120.PubMedPubMedCentral Ardeshir A, Narayan NR, Mendez-Lagares G, Lu D, Rauch M, Huang Y, et al. Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems. Sci Transl Med. 2014;6:252ra120.PubMedPubMedCentral
45.
Zurück zum Zitat Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol. 2012;9:565–76.PubMed Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol. 2012;9:565–76.PubMed
46.
Zurück zum Zitat Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010;156:3329–41.PubMed Roger LC, Costabile A, Holland DT, Hoyles L, McCartney AL. Examination of faecal Bifidobacterium populations in breast- and formula-fed infants during the first 18 months of life. Microbiology. 2010;156:3329–41.PubMed
47.
Zurück zum Zitat Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. Quantification of Bifidobacterium spp., Escherichiacoli and Clostridiumdifficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett. 2005;243:141–7.PubMed Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. Quantification of Bifidobacterium spp., Escherichiacoli and Clostridiumdifficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett. 2005;243:141–7.PubMed
48.
Zurück zum Zitat Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–94.PubMedPubMedCentral Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013;185:385–94.PubMedPubMedCentral
49.
Zurück zum Zitat Ianiro G, Tilg H, Gasbarrini A. Antibiotics as deep modulators of gut microbiota: between good and evil. Gut. 2016;65:1906–15.PubMed Ianiro G, Tilg H, Gasbarrini A. Antibiotics as deep modulators of gut microbiota: between good and evil. Gut. 2016;65:1906–15.PubMed
50.
Zurück zum Zitat Leclercq S, Mian FM, Stanisz AM, Bindels LB, Cambier E, Ben-Amram H, et al. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat Commun. 2017;8:15062.PubMedPubMedCentral Leclercq S, Mian FM, Stanisz AM, Bindels LB, Cambier E, Ben-Amram H, et al. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat Commun. 2017;8:15062.PubMedPubMedCentral
51.
Zurück zum Zitat Korpela K, Salonen A, Virta LJ, Kekkonen RA, Forslund K, Bork P, et al. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat Commun. 2016;7:10410.PubMedPubMedCentral Korpela K, Salonen A, Virta LJ, Kekkonen RA, Forslund K, Bork P, et al. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat Commun. 2016;7:10410.PubMedPubMedCentral
52.
Zurück zum Zitat Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Investig. 1996;98:945–53.PubMedPubMedCentral Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, et al. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Investig. 1996;98:945–53.PubMedPubMedCentral
53.
Zurück zum Zitat Sinkorova Z, Capkova J, Niederlova J, Stepankova R, Sinkora J. Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice. Hum Immunol. 2008;69:845–50.PubMed Sinkorova Z, Capkova J, Niederlova J, Stepankova R, Sinkora J. Commensal intestinal bacterial strains trigger ankylosing enthesopathy of the ankle in inbred B10.BR (H-2(k)) male mice. Hum Immunol. 2008;69:845–50.PubMed
54.
Zurück zum Zitat Longman RS, Littman DR. The functional impact of the intestinal microbiome on mucosal immunity and systemic autoimmunity. Curr Opin Rheumatol. 2015;27:381–7.PubMedPubMedCentral Longman RS, Littman DR. The functional impact of the intestinal microbiome on mucosal immunity and systemic autoimmunity. Curr Opin Rheumatol. 2015;27:381–7.PubMedPubMedCentral
55.
Zurück zum Zitat Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet. 2015;6:81.PubMedPubMedCentral Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet. 2015;6:81.PubMedPubMedCentral
56.
Zurück zum Zitat Yang L, Wang L, Wang X, Xian CJ, Lu H. A possible role of intestinal microbiota in the pathogenesis of ankylosing spondylitis. Int J Mol Sci. 2016;17:2126.PubMedCentral Yang L, Wang L, Wang X, Xian CJ, Lu H. A possible role of intestinal microbiota in the pathogenesis of ankylosing spondylitis. Int J Mol Sci. 2016;17:2126.PubMedCentral
57.
Zurück zum Zitat Picco P, Gattorno M, Marchese N, Vignola S, Sormani MP, Barabino A, et al. Increased gut permeability in juvenile chronic arthritides. A multivariate analysis of the diagnostic parameters. Clin Exp Rheumatol. 2000;18:773–8.PubMed Picco P, Gattorno M, Marchese N, Vignola S, Sormani MP, Barabino A, et al. Increased gut permeability in juvenile chronic arthritides. A multivariate analysis of the diagnostic parameters. Clin Exp Rheumatol. 2000;18:773–8.PubMed
58.
Zurück zum Zitat Weber P, Brune T, Ganser G, Zimmer KP. Gastrointestinal symptoms and permeability in patients with juvenile idiopathic arthritis. Clin Exp Rheumatol. 2003;21:657–62.PubMed Weber P, Brune T, Ganser G, Zimmer KP. Gastrointestinal symptoms and permeability in patients with juvenile idiopathic arthritis. Clin Exp Rheumatol. 2003;21:657–62.PubMed
59.
Zurück zum Zitat Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–98.PubMedPubMedCentral Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–98.PubMedPubMedCentral
60.
Zurück zum Zitat Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008;4:337–49.PubMedPubMedCentral Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe. 2008;4:337–49.PubMedPubMedCentral
61.
Zurück zum Zitat Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620–5.PubMed Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620–5.PubMed
62.
Zurück zum Zitat Yeoh N, Burton JP, Suppiah P, Reid G, Stebbings S. The role of the microbiome in rheumatic diseases. Curr Rheumatol Rep. 2013;15:314.PubMed Yeoh N, Burton JP, Suppiah P, Reid G, Stebbings S. The role of the microbiome in rheumatic diseases. Curr Rheumatol Rep. 2013;15:314.PubMed
63.
Zurück zum Zitat Littman DR, Rudensky AY. Th17 and regulatory T cells in mediating and restraining inflammation. Cell. 2010;140:845–58.PubMed Littman DR, Rudensky AY. Th17 and regulatory T cells in mediating and restraining inflammation. Cell. 2010;140:845–58.PubMed
64.
Zurück zum Zitat Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14:282–9.PubMed Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14:282–9.PubMed
65.
Zurück zum Zitat Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. The antibacterial lectin regIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science. 2011;334:255–8.PubMedPubMedCentral Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, et al. The antibacterial lectin regIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science. 2011;334:255–8.PubMedPubMedCentral
66.
Zurück zum Zitat Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13:321–35.PubMed Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13:321–35.PubMed
67.
Zurück zum Zitat Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, et al. ATP drives lamina propria T(H)17 cell differentiation. Nature. 2008;455:808–12.PubMed Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, et al. ATP drives lamina propria T(H)17 cell differentiation. Nature. 2008;455:808–12.PubMed
68.
Zurück zum Zitat Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149:1578–93.PubMedPubMedCentral Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012;149:1578–93.PubMedPubMedCentral
69.
Zurück zum Zitat Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol. 2009;39:2331–6.PubMed Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol. 2009;39:2331–6.PubMed
70.
Zurück zum Zitat Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337–41.PubMed Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337–41.PubMed
71.
Zurück zum Zitat Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34:794–806.PubMed Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34:794–806.PubMed
72.
Zurück zum Zitat Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–50.PubMed Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–50.PubMed
73.
Zurück zum Zitat Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 2010;107:12204–9.PubMedPubMedCentral Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 2010;107:12204–9.PubMedPubMedCentral
74.
Zurück zum Zitat Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332:974–7.PubMedPubMedCentral Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332:974–7.PubMedPubMedCentral
75.
Zurück zum Zitat Geuking MB, McCoy KD, Macpherson AJ. Metabolites from intestinal microbes shape Treg. Cell Res. 2013;23:1339–400.PubMedPubMedCentral Geuking MB, McCoy KD, Macpherson AJ. Metabolites from intestinal microbes shape Treg. Cell Res. 2013;23:1339–400.PubMedPubMedCentral
76.
Zurück zum Zitat Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73.PubMed Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569–73.PubMed
77.
78.
Zurück zum Zitat Wang Q, McLoughlin RM, Cobb BA, Charrel-Dennis M, Zaleski KJ, Golenbock D, et al. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J Exp Med. 2006;203:2853–63.PubMedPubMedCentral Wang Q, McLoughlin RM, Cobb BA, Charrel-Dennis M, Zaleski KJ, Golenbock D, et al. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J Exp Med. 2006;203:2853–63.PubMedPubMedCentral
79.
Zurück zum Zitat Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC, Kasper DL. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe. 2014;15:413–23.PubMedPubMedCentral Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC, Kasper DL. Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe. 2014;15:413–23.PubMedPubMedCentral
80.
Zurück zum Zitat den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–40. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013;54:2325–40.
81.
Zurück zum Zitat Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128–39.PubMedPubMedCentral Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, Shi H, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity. 2014;40:128–39.PubMedPubMedCentral
82.
Zurück zum Zitat Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504:451–5.PubMedPubMedCentral Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504:451–5.PubMedPubMedCentral
83.
Zurück zum Zitat Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, Porrett PM, et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med. 2007;13:1299–307.PubMed Tao R, de Zoeten EF, Ozkaynak E, Chen C, Wang L, Porrett PM, et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med. 2007;13:1299–307.PubMed
84.
Zurück zum Zitat Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe. 2013;14:559–70.PubMedPubMedCentral Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe. 2013;14:559–70.PubMedPubMedCentral
85.
Zurück zum Zitat Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336:489–93.PubMedPubMedCentral Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336:489–93.PubMedPubMedCentral
87.
Zurück zum Zitat Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–28.PubMed Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389:1218–28.PubMed
88.
Zurück zum Zitat Colman RJ, Rubin DT. Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis. 2014;8:1569–81.PubMed Colman RJ, Rubin DT. Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis. 2014;8:1569–81.PubMed
89.
Zurück zum Zitat Kragsnaes MS, Kjeldsen J, Horn HC, Munk HL, Pedersen FM, Holt HM, et al. Efficacy and safety of faecal microbiota transplantation in patients with psoriatic arthritis: protocol for a 6-month, double-blind, randomised, placebo-controlled trial. BMJ Open. 2018;8:e019231.PubMedPubMedCentral Kragsnaes MS, Kjeldsen J, Horn HC, Munk HL, Pedersen FM, Holt HM, et al. Efficacy and safety of faecal microbiota transplantation in patients with psoriatic arthritis: protocol for a 6-month, double-blind, randomised, placebo-controlled trial. BMJ Open. 2018;8:e019231.PubMedPubMedCentral
90.
Zurück zum Zitat De Palma G, Lynch MD, Lu J, Dang VT, Deng Y, Jury J, et al. Transplantation of fecal microbiota from patients with irritable bowel syndrome alters gut function and behavior in recipient mice. Sci Transl Med. 2017;9:eaaf6397.PubMed De Palma G, Lynch MD, Lu J, Dang VT, Deng Y, Jury J, et al. Transplantation of fecal microbiota from patients with irritable bowel syndrome alters gut function and behavior in recipient mice. Sci Transl Med. 2017;9:eaaf6397.PubMed
91.
Zurück zum Zitat Lai CY, Sung J, Cheng F, Tang W, Wong SH, Chan PKS, et al. Systematic review with meta-analysis: review of donor features, procedures and outcomes in 168 clinical studies of faecal microbiota transplantation. Aliment Pharmacol Ther. 2019;49:354–63.PubMed Lai CY, Sung J, Cheng F, Tang W, Wong SH, Chan PKS, et al. Systematic review with meta-analysis: review of donor features, procedures and outcomes in 168 clinical studies of faecal microbiota transplantation. Aliment Pharmacol Ther. 2019;49:354–63.PubMed
92.
Zurück zum Zitat Millar M, Seale J, Greenland M, Hardy P, Juszczak E, Wilks M, et al. The microbiome of infants recruited to a randomised placebo-controlled probiotic trial (PiPS trial). EBioMedicine. 2017;20:255–62.PubMedPubMedCentral Millar M, Seale J, Greenland M, Hardy P, Juszczak E, Wilks M, et al. The microbiome of infants recruited to a randomised placebo-controlled probiotic trial (PiPS trial). EBioMedicine. 2017;20:255–62.PubMedPubMedCentral
93.
Zurück zum Zitat Panigrahi P, Parida S, Nanda NC, Satpathy R, Pradhan L, Chandel DS, et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature. 2017;548:407–12.PubMed Panigrahi P, Parida S, Nanda NC, Satpathy R, Pradhan L, Chandel DS, et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature. 2017;548:407–12.PubMed
94.
Zurück zum Zitat Shukla A, Gaur P, Aggarwal A. Effect of probiotics on clinical and immune parameters in enthesitis-related arthritis category of juvenile idiopathic arthritis. Clin Exp Immunol. 2016;185:301–8.PubMedPubMedCentral Shukla A, Gaur P, Aggarwal A. Effect of probiotics on clinical and immune parameters in enthesitis-related arthritis category of juvenile idiopathic arthritis. Clin Exp Immunol. 2016;185:301–8.PubMedPubMedCentral
95.
Zurück zum Zitat Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. 2016;8:52.PubMedPubMedCentral Kristensen NB, Bryrup T, Allin KH, Nielsen T, Hansen TH, Pedersen O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials. Genome Med. 2016;8:52.PubMedPubMedCentral
96.
Zurück zum Zitat Ferrario C, Taverniti V, Milani C, Fiore W, Laureati M, De Noni I, et al. Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillusparacasei DG varies among healthy adults. J Nutr. 2014;144:1787–96.PubMed Ferrario C, Taverniti V, Milani C, Fiore W, Laureati M, De Noni I, et al. Modulation of fecal Clostridiales bacteria and butyrate by probiotic intervention with Lactobacillusparacasei DG varies among healthy adults. J Nutr. 2014;144:1787–96.PubMed
Metadaten
Titel
Intestinal microbiota and juvenile idiopathic arthritis: current understanding and future prospective
verfasst von
Le Xin
Feng He
Sen Li
Zhi-Xuan Zhou
Xiao-Lin Ma
Publikationsdatum
12.06.2020
Verlag
Springer Singapore
Erschienen in
World Journal of Pediatrics / Ausgabe 1/2021
Print ISSN: 1708-8569
Elektronische ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-020-00371-3

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