Microbial orchestra in juvenile idiopathic arthritis: Sounds of disarray?
Miika Arvonen
Department of Pediatrics, Kuopio University Hospital, University of Eastern Finland, Kuopio, Finland
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Search for more papers by this authorPetri Vänni
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Genobiomics LLC, Oulu, Finland
Search for more papers by this authorAditya Narayan Sarangi
Biomedical Informatics Center, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India
Search for more papers by this authorMysore V Tejesvi
Department of Ecology and Genetics, University of Oulu, Oulu, Finland
Genobiomics LLC, Oulu, Finland
Search for more papers by this authorPaula Vähäsalo
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Department of Children and Adolescents, Oulu University Hospital, Oulu, Finland
Medical Research Center Oulu, Oulu, Finland
Search for more papers by this authorAmita Aggarwal
Department of Clinical Immunology & Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India
Search for more papers by this authorCorresponding Author
Matthew L Stoll
Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL, USA
Correspondence
Matthew L Stoll, From the Department of Pediatrics at the University of Alabama at Birmingham, Birmingham, Alabama, USA.
Email: [email protected]
Search for more papers by this authorMiika Arvonen
Department of Pediatrics, Kuopio University Hospital, University of Eastern Finland, Kuopio, Finland
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Search for more papers by this authorPetri Vänni
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Genobiomics LLC, Oulu, Finland
Search for more papers by this authorAditya Narayan Sarangi
Biomedical Informatics Center, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India
Search for more papers by this authorMysore V Tejesvi
Department of Ecology and Genetics, University of Oulu, Oulu, Finland
Genobiomics LLC, Oulu, Finland
Search for more papers by this authorPaula Vähäsalo
PEDEGO Research Unit, Faculty of Medicine, University of Oulu, Oulu, Finland
Department of Children and Adolescents, Oulu University Hospital, Oulu, Finland
Medical Research Center Oulu, Oulu, Finland
Search for more papers by this authorAmita Aggarwal
Department of Clinical Immunology & Rheumatology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India
Search for more papers by this authorCorresponding Author
Matthew L Stoll
Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL, USA
Correspondence
Matthew L Stoll, From the Department of Pediatrics at the University of Alabama at Birmingham, Birmingham, Alabama, USA.
Email: [email protected]
Search for more papers by this authorAbstract
The role of the microbiota in multiple autoimmune diseases, including juvenile idiopathic arthritis (JIA) has earned substantial attention in the last 10 years. Increasing evidence suggests that the microbiota's link to JIA begins in early childhood, as early life events that influence the nature of the microbiota also appear to influence disease risk. In this review, we discuss these early life events including mode of delivery, infant feeding practice, antibiotics exposure, and other events and their impacts on the microbiota and on disease risk; reported abnormalities of the microbiota in children with JIA; mechanisms by which an altered microbiota at birth and later on in childhood may influence disease risk; and the prospects for therapeutic alteration of the microbiota in children with JIA.
REFERENCES
- 1Bodansky HJ, Staines A, Stephenson C, Haigh D, Cartwright R. Evidence for an environmental effect in the aetiology of insulin dependent diabetes in a transmigratory population. BMJ. 1992; 304: 1020-1022.
- 2Ahlgren C, Oden A, Lycke J. A nationwide survey of the prevalence of multiple sclerosis in immigrant populations of Sweden. Mult Scler. 2012; 18: 1099-1107.
- 3Benchimol EI, Mack DR, Guttmann A, et al. Inflammatory bowel disease in immigrants to Canada and their children: a population-based cohort study. Am J Gastroenterol. 2015; 110: 553-563.
- 4De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010; 107: 14691-14696.
- 5Brandtzaeg P. Homeostatic impact of indigenous microbiota and secretory immunity. Benef Microbes. 2010; 1: 211-227.
- 6Tejesvi MV, Arvonen M, Kangas SM, et al. Faecal microbiome in new-onset juvenile idiopathic arthritis. Eur J Clin Microbiol Infect Dis. 2016; 35(3): 363-370.
- 7Aggarwal 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: 480-489.
- 8Stoll ML, Kumar R, Morrow CD, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther. 2014; 16(6): 486.
- 9Cole JR, Wang Q, Fish JA, et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014; 42: D633-D642.
- 10Rognes T, Flouri T, Nichols B, Quince C, Mahe F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016; 4:e2584.
- 11Lawley B, Tannock GW. Analysis of 16S rRNA gene amplicon sequences using the QIIME software package. Methods Mol Biol. 2017; 1537: 153-163.
- 12Pedregosa F, Varoquaux G, Gramfort A, et al. Scikit-learn: machine Learning in Python. J Mach Learn Res. 2011; 12: 2825-2830.
- 13Breiman L. Random Forests. Mach Learn. 2001; 45: 5-32.
- 14Hunter J. Matplotlib: a 2D graphics environment. Comput Sci Eng. 2007; 9: 90-95.
- 15Carlens 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: 1159-1164.
- 16Kristensen K, Henriksen L. Cesarean section and disease associated with immune function. J Allergy Clin Immunol. 2016; 137: 587-590.
- 17Bell SW, Shenoi S, Nelson JL, Bhatti P, Mueller BA. Juvenile idiopathic arthritis in relation to perinatal and maternal characteristics: a case control study. Pediatr Rheumatol Online J. 2017; 15(1): 36.
- 18Cho CE, Norman M. Cesarean section and development of the immune system in the offspring. Am J Obstet Gynecol. 2013; 208: 249-254.
- 19Biasucci G, Rubini M, Riboni S, Morelli L, Bessi E, Retetangos C. Mode of delivery affects the bacterial community in the newborn gut. Early Hum Dev. 2010; 86(Suppl 1): 13-15.
- 20Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants' life: a systematic review. BMC Gastroenterol. 2016; 16(1).
- 21Shao Y, Forster SC, Tsaliki E, et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019.
- 22Azad MB, Konya T, Maughan H, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ. 2013; 185: 385-394.
- 23Fouhy F, Watkins C, Hill CJ, et al. Perinatal factors affect the gut microbiota up to four years after birth. Nat Commun. 2019; 10: 1517.
- 24Tapiainen T, Koivusaari P, Brinkac L, et al. Impact of intrapartum and postnatal antibiotics on the gut microbiome and emergence of antimicrobial resistance in infants. Sci Rep. 2019; 9(1): 10635.
- 25Wampach L, Heintz-Buschart A, Hogan A, et al. Colonization and succession within the human gut microbiome by Archaea, Bacteria, and Microeukaryotes during the first year of life. Front Microbiol. 2017; 8: 738.
- 26Dominguez-Bello MG, Costello EK, Contreras M, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010; 107: 11971-11975.
- 27Goedert JJ, Hua X, Yu G, Shi J. Diversity and composition of the adult fecal microbiome associated with history of cesarean birth or appendectomy: analysis of the American Gut Project. EBioMedicine. 2014; 1: 167-172.
- 28Hesla HM, Stenius F, Jaderlund L, et al. Impact of lifestyle on the gut microbiota of healthy infants and their mothers-the ALADDIN birth cohort. FEMS Microbiol Ecol. 2014; 90: 791-801.
- 29Chu 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: 314-326.
- 30El Aidy S, Hooiveld G, Tremaroli V, Backhed F, Kleerebezem M. The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter? Gut Microbes. 2013; 4: 118-124.
- 31El Aidy S, van Baarlen P, Derrien M, et al. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol. 2012; 5: 567-579.
- 32Mason T, Rabinovich CE, Fredrickson DD, et al. Breast feeding and the development of juvenile rheumatoid arthritis. J Rheumatol. 1995; 22: 1166-1170.
- 33Kasapcopur O, Tasdan Y, Apelyan M, et al. Does breast feeding prevent the development of juvenile rheumatoid arthritis? J Rheumatol. 1998; 25: 2286-2287.
- 34Rosenberg AM. Evaluation of associations between breast feeding and subsequent development of juvenile rheumatoid arthritis. J Rheumatol. 1996; 23: 1080-1082.
- 35Hyrich KL, Baildam E, Pickford H, et al. Influence of past breast feeding on pattern and severity of presentation of juvenile idiopathic arthritis. Arch Dis Child. 2016; 101: 348-351.
- 36Kindgren 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(1): 46.
- 37Montoya J, Matta NB, Suchon P, et al. Patients with ankylosing spondylitis have been breast fed less often than healthy controls: a case-control retrospective study. Ann Rheum Dis. 2016; 75: 879-882.
- 38Berntson L, Andersson Gare B, Fasth A, et al. Incidence of juvenile idiopathic arthritis in the Nordic countries. A population based study with special reference to the validity of the ILAR and EULAR criteria. J Rheumatol. 2003; 30: 2275-2282.
- 39Moossavi S, Sepehri S, Robertson B, et al. Composition and variation of the human milk microbiota are influenced by maternal and early-life factors. Cell Host Microbe. 2019; 25(2): 324–335.e4.
- 40Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol. 2012; 9: 565-576.
- 41Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr. 2000; 30: 61-67.
- 42Bunesova V, Lacroix C, Schwab C. Mucin cross-feeding of infant Bifidobacteria and Eubacterium hallii. Microb Ecol. 2018; 75: 228-238.
- 43Kumar A, Alrefai WA, Borthakur A, Dudeja PK. Lactobacillus acidophilus counteracts enteropathogenic E. coli-induced inhibition of butyrate uptake in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2015; 309: G602-G607.
- 44Verduci E, Banderali G, Barberi S, et al. Epigenetic effects of human breast milk. Nutrients. 2014; 6: 1711-1724.
- 45Perez PF, Dore J, Leclerc M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007; 119: e724-e732.
- 46Bhinder G, Allaire JM, Garcia C, et al. Milk fat globule membrane supplementation in formula modulates the neonatal gut microbiome and normalizes intestinal development. Sci Rep. 2017; 7: 45274.
- 47Mielants H, Veys EM, Cuvelier C, et al. Gut inflammation in children with late onset pauciarticular juvenile chronic arthritis and evolution to adult spondyloarthropathy–a prospective study. J Rheumatol. 1993; 20: 1567-1572.
- 48Stoll ML, Punaro M, Patel AS. Fecal calprotectin in children with the enthesitis-related arthritis subtype of juvenile idiopathic arthritis. J Rheumatol. 2011; 38: 2274-2275.
- 49Wallis D, Asaduzzaman A, Weisman M, et al. Elevated serum anti-flagellin antibodies implicate subclinical bowel inflammation in ankylosing spondylitis: an observational study. Arthritis Res Ther. 2013; 15: R166.
- 50Korpela K, Salonen A, Virta LJ, Kekkonen RA, de Vos WM. Association of early-life antibiotic use and protective effects of breastfeeding: role of the intestinal microbiota. JAMA Pediatr. 2016; 170: 750-757.
- 51Horton DB, Scott FI, Haynes K, et al. Antibiotic exposure and juvenile idiopathic arthritis: a case-control study. Pediatrics. 2015; 136: e333-e343.
- 52Arvonen 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(3): 521-526.
- 53Lavelle A, Hoffmann TW, Pham HP, Langella P, Guedon E, Sokol H. Baseline microbiota composition modulates antibiotic-mediated effects on the gut microbiota and host. Microbiome. 2019; 7(1): 111.
- 54Arvonen 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(1): 44.
- 55Panda S, El khader I, Casellas F, et al. Short-term effect of antibiotics on human gut microbiota. PLoS ONE. 2014; 9:e95476.
- 56Jernberg C, Lofmark S, Edlund C, Jansson JK. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007; 1: 56-66.
- 57Di Paola M, Cavalieri D, Albanese D, et al. Alteration of fecal microbiota profiles in juvenile idiopathic arthritis. associations with HLA-B27 allele and disease status. Front Microbiol. 2016; 7: 1703.
- 58Mosca A, Leclerc M, Hugot JP. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? Front Microbiol. 2016; 7: 455.
- 59Nielsen HE, Dorup J, Herlin T, Larsen K, Nielsen S, Pedersen FK. Epidemiology of juvenile chronic arthritis: risk dependent on sibship, parental income, and housing. J Rheumatol. 1999; 26: 1600-1605.
- 60Radon K, Windstetter D, Poluda D, et al. Exposure to animals and risk of oligoarticular juvenile idiopathic arthritis: a multicenter case-control study. BMC Musculoskelet Disord. 2010; 11(1): 73.
- 61Shenoi S, Shaffer ML, Wallace CA. Environmental risk factors and early-life exposures in juvenile idiopathic arthritis: a case-control study. Arthritis Care Res (Hoboken). 2016; 68: 1186-1194.
- 62Lane AA, McGuire MK, McGuire MA, et al. Household composition and the infant fecal microbiome: the INSPIRE study. Am J Phys Anthropol. 2019; 169: 526-539.
- 63Miller J, Ponsonby AL, Pezic A, et al. Sibling exposure and risk of juvenile idiopathic arthritis. Arthritis Rheumatol. 2015; 67: 1951-1958.
- 64Prahalad S, Fraser AM, O'Brien E, Kerber RA, Mineau GP, Bohnsack JF. Lack of association between birth order and juvenile idiopathic arthritis. Arthritis Rheum. 2003; 48: 2989-2990.
- 65Chernikova DA, Madan JC, Housman ML, et al. The premature infant gut microbiome during the first 6 weeks of life differs based on gestational maturity at birth. Pediatr Res. 2018; 84: 71-79.
- 66Zhao Q, Elson CO. Adaptive immune education by gut microbiota antigens. Immunology. 2018; 154: 28-37.
- 67Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Science. 2016; 352: 539-544.
- 68Renz H, Brandtzaeg P, Hornef M. The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol. 2011; 12: 9-23.
- 69Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol. 2010; 10: 159-169.
- 70Round JL, Lee SM, Li J, et al. The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011; 332: 974-977.
- 71Van Praet JT, Donovan E, Vanassche I, et al. Commensal microbiota influence systemic autoimmune responses. EMBO J. 2015; 34: 466-474.
- 72Zonneveld-Huijssoon E, van Wijk F, Roord S, et al. TLR9 agonist CpG enhances protective nasal HSP60 peptide vaccine efficacy in experimental autoimmune arthritis. Ann Rheum Dis. 2012; 71(10): 1706-1715.
- 73Mathis D, Benoist C. Microbiota and autoimmune disease: the hosted self. Cell Host Microbe. 2011; 10: 297-301.
- 74Faith JJ, Ahern PP, Ridaura VK, Cheng J, Gordon JI. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci Transl Med. 2014; 6: 220ra11.
- 75Atarashi K, Tanoue T, Oshima K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature. 2013; 500: 232-236.
- 76Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011; 331: 337-341.
- 77Atarashi K, Tanoue T, Ando M, et al. Th17 cell induction by adhesion of microbes to intestinal epithelial cells. Cell. 2015; 163: 367-380.
- 78Legoux F, Bellet D, Daviaud C, et al. Microbial metabolites control the thymic development of mucosal-associated invariant T cells. Science. 2019.
- 79Taurog JD, Richardson JA, Croft JT, et al. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med. 1994; 180: 2359-2364.
- 80Wu HJ, Ivanov II, Darce J, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity. 2010; 32: 815-827.
- 81Sinkorova 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: 845-850.
- 82Vatanen T, Kostic AD, d'Hennezel E, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell. 2016; 165: 842-853.
- 83Malievskiy V. Prevalence and incidence of juvenile idiopathic arthritis in children in the republic of Bashkortostan: the epidemiological study. PROJ. 2011; 9(Suppl 1): 145.
- 84Pruunsild C, Uibo K, Liivamagi H, Tarraste S, Talvik T, Pelkonen P. Incidence of juvenile idiopathic arthritis in children in Estonia: a prospective population-based study. Scand J Rheumatol. 2007; 36: 7-13.
- 85Virta L, Helenius H, Klaukka T. Incidence of Juvenile idiopathic arthritis is increasing in Finland [In Finnish]. Suomen Lääkärilehti. 2008; 35: 2806-2809.
- 86Rautava S, Ruuskanen O, Ouwehand A, Salminen S, Isolauri E. The hygiene hypothesis of atopic disease–an extended version. J Pediatr Gastroenterol Nutr. 2004; 38: 378-388.
- 87Torow N, Hornef MW. The neonatal window of opportunity: setting the stage for life-long host-microbial interaction and immune homeostasis. J Immunol. 2017; 198: 557-563.
- 88Cahenzli 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: 559-570.
- 89Olszak T, An D, Zeissig S, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012; 336: 489-493.
- 90Hagan T, Cortese M, Rouphael N, et al. Antibiotics-driven gut microbiome perturbation alters immunity to vaccines in humans. Cell. 2019; 178(6): 1313–1328.e13.
- 91van Dijkhuizen EHP, Del Chierico F, Malattia C, et al. Microbiome analytics of the gut microbiota in patients with juvenile idiopathic arthritis: a longitudinal observational cohort study. Arthritis Rheumatol. 2019; 71: 1000-1010.
- 92Hissink Muller PCE, Westedt PM, Budding AE, et al. Disturbance of microbial core species in new-onset juvenile idiopathic arthritis. J Pediatr Infect Dis. 2017; 12: 131-135.
- 93Stoll ML, Weiss PF, Weiss JE, et al. Age and fecal microbial strain-specific differences in patients with spondyloarthritis. Arthritis Res Ther. 2018; 20: 14.
- 94Kolho KL, Korpela K, Jaakkola T, et al. Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am J Gastroenterol. 2015; 110: 921-930.
- 95Chen L, Wang W, Zhou R, et al. Characteristics of fecal and mucosa-associated microbiota in Chinese patients with inflammatory bowel disease. Medicine (Baltimore). 2014; 93: e51.
- 96Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012; 13: R79.
- 97Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014; 15: 382-392.
- 98El Mouzan M, Wang F, Al Mofarreh M, et al. Fungal Microbiota Profile in Newly Diagnosed Treatment-naive Children with Crohn's Disease. J Crohns Colitis. 2017; 11: 586-592.
- 99Nagata N, Tohya M, Fukuda S, et al. Effects of bowel preparation on the human gut microbiome and metabolome. Sci Rep. 2019; 9: 4042.
- 100Levy SE, Myers RM. Advancements in next-generation sequencing. Annu Rev Genomics Hum Genet. 2016; 17: 95-115.
- 101Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. Review article: the role of butyrate on colonic function. Aliment Pharmacol Ther. 2008; 27: 104-119.
- 102Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013; 341: 569-573.
- 103Stoll ML, Kumar R, Lefkowitz EJ, Cron RQ, Morrow CD, Barnes S. Fecal metabolomics in pediatric spondyloarthritis implicate decreased metabolic diversity and altered tryptophan metabolism as pathogenic factors. Genes Immun. 2016; 17(7): 400–405.
- 104Breban M, Tap J, Leboime A, et al. Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann Rheum Dis. 2017; 76: 1614-1622.
- 105Tailford LE, Crost EH, Kavanaugh D, Juge N. Mucin glycan foraging in the human gut microbiome. Front Genet. 2015; 6: 81.
- 106Giongo A, Gano KA, Crabb DB, et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2011; 5: 82-91.
- 107Zhou Y, Zhi F. Lower level of bacteroides in the gut microbiota is associated with inflammatory bowel disease: a meta-analysis. Biomed Res Int. 2016; 2016: 5828959.
- 108Scher JU, Sczesnak A, Longman RS, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013; 2:e01202.
- 109Stebbings S, Munro K, Simon MA, et al. Comparison of the faecal microflora of patients with ankylosing spondylitis and controls using molecular methods of analysis. Rheumatology (Oxford). 2002; 41: 1395-1401.
- 110Tito RY, Cypers H, Joossens M, et al. Brief report: dialister as a microbial marker of disease activity in spondyloarthritis. Arthritis Rheumatol. 2017; 69: 114-121.
- 111Scher JU, Ubeda C, Artacho A, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015; 67: 128-139.
- 112Shah R, Cope JL, Nagy-Szakal D, et al. Composition and function of the pediatric colonic mucosal microbiome in untreated patients with ulcerative colitis. Gut Microbes. 2016; 7: 384-396.
- 113Ganesh BP, Klopfleisch R, Loh G, Blaut M. Commensal akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLoS ONE. 2013; 8:e74963.
- 114Asquith 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: 2151-2162.
- 115Stoll ML, Pierce MK, Watkins JA, et al. Akkermansia muciniphila is permissive to arthritis in the K/BxN mouse model of arthritis. Genes Immun. 2019; 20: 158-166.
- 116Rashid T, Ebringer A, Wilson C. The link between klebsiella and ankylosing spondylitis in worldwide geographical locations. Curr Rheumatol Rev. 2016; 12: 223-231.
- 117Cypers H, Bridges SL, Elewaut D. Spondyloarthritis. In: G Ragab, P Atkinson, ML Stoll, eds. The Microbiota in Rheumatic Diseases and Infection, 1st edn. Cham: Springer; 2018: 201-220.
10.1007/978-3-319-79026-8_16 Google Scholar
- 118Saxena N, Misra R, Aggarwal A. Is the enthesitis-related arthritis subtype of juvenile idiopathic arthritis a form of chronic reactive arthritis? Rheumatology (Oxford). 2006; 45: 1129-1132.
- 119Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol. 2014; 6: 703-713.
- 120Tamanai-Shacoori Z, Smida I, Bousarghin L, et al. Roseburia spp.: a marker of health? Future Microbiol. 2017; 12: 157-170.
- 121Bailey CF. The treatment of chronic rheumatic and rheumatoid arthritis by radiant heat and cataphoresis. Br Med J. 1909; 1: 13-15.
- 122Mayberry J. The history of 5-ASA compounds and their use in ulcerative colitis–trailblazing discoveries in gastroenterology. J Gastrointestin Liver Dis. 2013; 22: 375-377.
- 123Stoll ML, Bridges SL Jr, Danila ML. Rheumatoid arthritis. In: G Ragab, P Atkinson, ML Stoll, eds. The Microbiota in Rheumatic Diseases and Infection, 1st edn. Cham: Springer; 2018: 183-199.
10.1007/978-3-319-79026-8_15 Google Scholar
- 124Nordstrom D, Lindy O, Lauhio A, Sorsa T, Santavirta S, Konttinen YT. Anti-collagenolytic mechanism of action of doxycycline treatment in rheumatoid arthritis. Rheumatol Int. 1998; 17: 175-180.
- 125O'Dell JR, Elliott JR, Mallek JA, et al. Treatment of early seropositive rheumatoid arthritis: doxycycline plus methotrexate versus methotrexate alone. Arthritis Rheum. 2006; 54: 621-627.
- 126Kolacek S, Hojsak I, Berni Canani R, et al. Commercial probiotic products: a call for improved quality control. A position paper by the ESPGHAN working group for probiotics and prebiotics. J Pediatr Gastroenterol Nutr. 2017; 65: 117-124.
- 127Shukla 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: 301-308.
- 128Jenks K, Stebbings S, Burton J, Schultz M, Herbison P, Highton J. Probiotic therapy for the treatment of spondyloarthritis: a randomized controlled trial. J Rheumatol. 2010; 37: 2118-2125.
- 129Brophy S, Burrows CL, Brooks C, Gravenor MB, Siebert S, Allen SJ. Internet-based randomised controlled trials for the evaluation of complementary and alternative medicines: probiotics in spondyloarthropathy. BMC Musculoskelet Disord. 2008; 9: 4.
- 130Alipour B, Homayouni-Rad A, Vaghef-Mehrabany E, et al. Effects of Lactobacillus casei supplementation on disease activity and inflammatory cytokines in rheumatoid arthritis patients: a randomized double-blind clinical trial. Int J Rheum Dis. 2014; 17: 519-527.
- 131Hatakka K, Martio J, Korpela M, et al. Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis–a pilot study. Scand J Rheumatol. 2003; 32: 211-215.
- 132Pineda Mde L, Thompson SF, Summers K, de Leon F, Pope J, Reid G. A randomized, double-blinded, placebo-controlled pilot study of probiotics in active rheumatoid arthritis. Med Sci Monit. 2011; 17: CR347-CR354.
- 133Moens F, Van den Abbeele P, Basit AW, et al. A four-strain probiotic exerts positive immunomodulatory effects by enhancing colonic butyrate production in vitro. Int J Pharm. 2019; 555: 1-10.
- 134Zmora N, Zilberman-Schapira G, Suez J, et al. Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell. 2018; 174: 1388-1405.e21.
- 135Keshteli AH, Millan B, Madsen KL. Pretreatment with antibiotics may enhance the efficacy of fecal microbiota transplantation in ulcerative colitis: a meta-analysis. Mucosal Immunol. 2017; 10: 565-566.
- 136Yu Y, Chen KC, Chen J. Exclusive enteral nutrition versus corticosteroids for treatment of pediatric Crohn's disease: a meta-analysis. World J Pediatr. 2019; 15: 26-36.
- 137Sigall-Boneh R, Pfeffer-Gik T, Segal I, Zangen T, Boaz M, Levine A. Partial enteral nutrition with a Crohn's disease exclusion diet is effective for induction of remission in children and young adults with Crohn's disease. Inflamm Bowel Dis. 2014; 20: 1353-1360.
- 138Svolos V, Hansen R, Nichols B, et al. Treatment of active Crohn's disease with an ordinary food-based diet that replicates exclusive enteral nutrition. Gastroenterology. 2019; 156: 1354–1367.e6.
- 139Levine A, Wine E, Assa A, et al. Crohn's disease exclusion diet plus partial enteral nutrition induces sustained remission in a randomized controlled trial. Gastroenterology. 2019; 157(2): 440–450.e8.
- 140Gerasimidis K, Bertz M, Hanske L, et al. Decline in presumptively protective gut bacterial species and metabolites are paradoxically associated with disease improvement in pediatric Crohn's disease during enteral nutrition. Inflamm Bowel Dis. 2014; 20: 861-871.
- 141Berntson L. Anti-inflammatory effect by exclusive enteral nutrition (EEN) in a patient with juvenile idiopathic arthritis (JIA): brief report. Clin Rheumatol. 2014; 33(8): 1173–1175.
- 142Berntson L, Hedlund-Treutiger I, Alving K. Anti-inflammatory effect of exclusive enteral nutrition in patients with juvenile idiopathic arthritis. Clin Exp Rheumatol. 2016; 34: 941-945.
- 143Berntson 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: 1501-1506.
- 144Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. Microbial degradation of complex carbohydrates in the gut. Gut Microbes. 2012; 3: 289-306.
- 145Moens F, De Vuyst L. Inulin-type fructan degradation capacity of Clostridium cluster IV and XIVa butyrate-producing colon bacteria and their associated metabolic outcomes. Benef Microbes. 2017; 8: 473-490.
- 146Asquith M, Davin S, Stauffer 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: 1984-1995.
- 147Wedlake L, Slack N, Andreyev HJ, Whelan K. Fiber in the treatment and maintenance of inflammatory bowel disease: a systematic review of randomized controlled trials. Inflamm Bowel Dis. 2014; 20: 576-586.
- 148Weaver CT, Elson CO, Fouser LA, Kolls JK. The Th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu Rev Pathol. 2013; 8: 477-512.
- 149Kleinewietfeld M, Manzel A, Titze J, et al. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature. 2013; 496: 518-522.
- 150Wu C, Yosef N, Thalhamer T, et al. Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature. 2013; 496: 513-517.
- 151Aguiar SLF, Miranda MCG, Guimaraes MAF, et al. High-salt diet induces IL-17-dependent gut inflammation and exacerbates colitis in mice. Front Immunol. 2018; 8: 1969.
- 152Jung SM, Kim Y, Kim J, et al. Sodium chloride aggravates arthritis via Th17 polarization. Yonsei Med J. 2019; 60: 88-97.
- 153Scrivo R, Massaro L, Barbati C, et al. The role of dietary sodium intake on the modulation of T helper 17 cells and regulatory T cells in patients with rheumatoid arthritis and systemic lupus erythematosus. PLoS ONE. 2017; 12:e0184449.
- 154Damas OM, Garces L, Abreu MT. Diet as adjunctive treatment for inflammatory bowel disease: review and update of the latest literature. Curr Treat Options Gastroenterol. 2019; 17: 313-325.
- 155Burgis JC, Nguyen K, Park KT, Cox K. Response to strict and liberalized specific carbohydrate diet in pediatric Crohn's disease. World J Gastroenterol. 2016; 22: 2111-2117.
- 156Obih C, Wahbeh G, Lee D, et al. Specific carbohydrate diet for pediatric inflammatory bowel disease in clinical practice within an academic IBD center. Nutrition. 2016; 32: 418-425.
- 157Cohen SA, Gold BD, Oliva S, et al. Clinical and mucosal improvement with specific carbohydrate diet in pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 2014; 59: 516-521.
- 158Suskind DL, Cohen SA, Brittnacher MJ, et al. Clinical and fecal microbial changes with diet therapy in active inflammatory bowel disease. J Clin Gastroenterol. 2018; 52: 155-163.
- 159Arvonen M, Vahasalo P, Turunen S, et al. Altered expression of intestinal human leucocyte antigen D-related and immune signalling molecules in juvenile idiopathic arthritis. Clin Exp Immunol. 2012; 170: 266-273.
- 160Hagen KB, Byfuglien MG, Falzon L, Olsen SU, Smedslund G. Dietary interventions for rheumatoid arthritis. Cochrane Database Syst Rev. 2009;(1): CD006400. http://CD006400.
- 161Eiseman B, Silen W, BASCOM GS, KAUVAR AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958; 44: 854-859.
- 162Fischer M, Kao D, Kelly C, et al. Fecal microbiota transplantation is safe and efficacious for recurrent or refractory Clostridium difficile Infection in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016; 22: 2402-2409.
- 163Zhang FM, Wang HG, Wang M, Cui BT, Fan ZN, Ji GZ. Fecal microbiota transplantation for severe enterocolonic fistulizing Crohn's disease. World J Gastroenterol. 2013; 19: 7213-7216.
- 164Borody TJ, Warren EF, Leis S, Surace R, Ashman O. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol. 2003; 37: 42-47.
- 165DeFilipp Z, Bloom PP, Soto MT, et al. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N Engl J Med. 2019; 381: 2043–2050.
- 166Zhu W, Winter MG, Byndloss MX, et al. Precision editing of the gut microbiota ameliorates colitis. Nature. 2018; 553: 208-211.
- 167Cieplak T, Soffer N, Sulakvelidze A, Nielsen DS. A bacteriophage cocktail targeting Escherichia coli reduces E. coli in simulated gut conditions, while preserving a non-targeted representative commensal normal microbiota. Gut Microbes. 2018; 9: 391-399.
- 168Pursey E, Sunderhauf D, Gaze WH, Westra ER, van Houte S. CRISPR-Cas antimicrobials: challenges and future prospects. PLoS Pathog. 2018; 14:e1006990.
- 169Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016; 22: 250-253.
- 170 Committee on Obstetric Practice. Committee opinion no. 725: vaginal seeding. Obstet Gynecol. 2017; 130: e274-e278.
- 171Goossens H, Ferech M, Vander Stichele R, Elseviers M, and ESAC Project Group. Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet. 2005; 365: 579-587.
- 172Virta L, Auvinen A, Helenius H, Huovinen P, Kolho KL. Association of repeated exposure to antibiotics with the development of pediatric Crohn's disease–a nationwide, register-based finnish case-control study. Am J Epidemiol. 2012; 175: 775-784.
- 173Sultan AA, Mallen C, Muller S, et al.Antibiotic use and the risk of rheumatoid arthritis: a population-based case-control study. BMC Med. 2019; 17: 1-9.