Role of Intestinal Dysbiosis and Nutrition in Rheumatoid Arthritis
Abstract
:1. Introduction
2. What Is the Gut Microbiome?
2.1. Development of the Gut Microbiome
2.2. Gut Microbiome Function
3. Microbiota in Rheumatoid Arthritis
3.1. Experimental Animal Models
3.2. CIA Model
3.3. SKG Model
3.4. K/BxN Model
3.5. IL1rn -/- Model
4. Human RA Studies
5. Rheumatoid Arthritis and Nutrition
5.1. Mediterranean Diet
5.2. Dietary Regimens
5.3. Other Dietary Factors
6. Therapeutics Targeted toward Dysbiosis
6.1. Probiotics
6.2. Fermented Food
6.3. Microbiome-Derived Metabolites
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Peroumal, D.; Abimannan, T.; Tagirasa, R.; Parida, J.R.; Singh, S.K.; Padhan, P.; Devadas, S. Inherent low Erk and p38 activity reduce Fas Ligand expression and degranulation in T helper 17 cells leading to activation induced cell death resistance. Oncotarget 2016, 7, 54339–54359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, K.; Bang, S.Y.; Lee, H.S.; Bae, S.C. Update on the genetic architecture of rheumatoid arthritis. Nat. Rev. Rheumatol. 2017, 13, 13–24. [Google Scholar] [CrossRef]
- MacGregor, A.J.; Snieder, H.; Rigby, A.S.; Koskenvuo, M.; Kaprio, J.; Aho, K.; Silman, A.J. Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins. Arthritis Rheum. 2000, 43, 30–37. [Google Scholar] [CrossRef]
- Silman, A.J.; MacGregor, A.J.; Thomson, W.; Holligan, S.; Carthy, D.; Farhan, A.; Ollier, W.E. Twin concordance rates for rheumatoid arthritis: Results from a nationwide study. Br. J. Rheumatol. 1993, 32, 903–907. [Google Scholar] [CrossRef] [PubMed]
- McInnes, I.B.; Schett, G. The pathogenesis of rheumatoid arthritis. N. Engl. J. Med. 2011, 365, 2205–2219. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mazmanian, S.K.; Liu, C.H.; Tzianabos, A.O.; Kasper, D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122, 107–118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rakoff-Nahoum, S.; Paglino, J.; Eslami-Varzaneh, F.; Edberg, S.; Medzhitov, R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118, 229–241. [Google Scholar] [CrossRef] [Green Version]
- Bodkhe, R.; Balakrishnan, B.; Taneja, V. The role of microbiome in rheumatoid arthritis treatment. Ther. Adv. Musculoskelet. Dis. 2019, 11, 1759720x19844632. [Google Scholar] [CrossRef]
- Baquero, F.; Nombela, C. The microbiome as a human organ. Clin. Microbiol. Infect. 2012, 18 (Suppl. 4), 2–4. [Google Scholar] [CrossRef] [Green Version]
- Berg, G.; Rybakova, D.; Fischer, D.; Cernava, T.; Verges, M.C.; Charles, T.; Chen, X.; Cocolin, L.; Eversole, K.; Corral, G.H.; et al. Microbiome definition re-visited: Old concepts and new challenges. Microbiome 2020, 8, 103. [Google Scholar]
- Wassenaar, T.M.; Panigrahi, P. Is a foetus developing in a sterile environment? Lett. Appl. Microbiol. 2014, 59, 572–579. [Google Scholar] [CrossRef] [PubMed]
- Ardissone, A.N.; de la Cruz, D.M.; Davis-Richardson, A.G.; Rechcigl, K.T.; Li, N.; Drew, J.C.; Murgas-Torrazza, R.; Sharma, R.; Hudak, M.L.; Triplett, E.W.; et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS ONE 2014, 9, e90784. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dominguez-Bello, M.G.; Costello, E.K.; Contreras, M.; Magris, M.; Hidalgo, G.; Fierer, N.; Knight, R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA 2010, 107, 11971–11975. [Google Scholar] [CrossRef] [Green Version]
- Arumugam, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D.R.; Fernandes, G.R.; Tap, J.; Bruls, T.; Batto, J.M.; et al. Enterotypes of the human gut microbiome. Nature 2011, 473, 174–180. [Google Scholar] [CrossRef]
- 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]
- Barko, P.C.; McMichael, M.A.; Swanson, K.S.; Williams, D.A. The Gastrointestinal Microbiome: A Review. J. Vet. Intern. Med. 2018, 32, 9–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, K. Strategies to promote abundance of Akkermansia muciniphila, an emerging probiotics in the gut, evidence from dietary intervention studies. J. Funct. Foods 2017, 33, 194–201. [Google Scholar] [CrossRef]
- Sun, Y.; Chen, Q.; Lin, P.; Xu, R.; He, D.; Ji, W.; Bian, Y.; Shen, Y.; Li, Q.; Liu, C.; et al. Characteristics of Gut Microbiota in Patients with Rheumatoid Arthritis in Shanghai, China. Front. Cell. Infect. Microbiol. 2019, 9, 369. [Google Scholar] [CrossRef] [Green Version]
- Schade, L.; Mesa, D.; Faria, A.R.; Santamaria, J.R.; Xavier, C.A.; Ribeiro, D.; Hajar, F.N.; Azevedo, V.F. The gut microbiota profile in psoriasis: A Brazilian case-control study. Lett. Appl. Microbiol. 2022, 74, 498–504. [Google Scholar] [CrossRef]
- Scher, J.U.; Ubeda, C.; Artacho, A.; Attur, M.; Isaac, S.; Reddy, S.M.; Marmon, S.; Neimann, A.; Brusca, S.; Patel, T.; 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. [Google Scholar] [CrossRef] [Green Version]
- Hamazaki, M.; Sawada, T.; Yamamura, T.; Maeda, K.; Mizutani, Y.; Ishikawa, E.; Furune, S.; Yamamoto, K.; Ishikawa, T.; Kakushima, N.; et al. Fecal microbiota transplantation in the treatment of irritable bowel syndrome: A single-center prospective study in Japan. BMC Gastroenterol. 2022, 22, 342. [Google Scholar] [CrossRef]
- Wang, L.; Wang, Y.; Zhang, P.; Song, C.; Pan, F.; Li, G.; Peng, L.; Yang, Y.; Wei, Z.; Huang, F. Gut microbiota changes in patients with spondyloarthritis: A systematic review. Semin. Arthritis Rheum. 2022, 52, 151925. [Google Scholar] [CrossRef] [PubMed]
- Liu, F.; Ren, T.; Li, X.; Zhai, Q.; Xu, X.; Zhang, N.; Jiang, P.; Niu, Y.; Lv, L.; Shi, G.; et al. Distinct Microbiomes of Gut and Saliva in Patients with Systemic Lupus Erythematous and Clinical Associations. Front. Immunol. 2021, 12, 626217. [Google Scholar] [CrossRef] [PubMed]
- den Besten, G.; van Eunen, K.; Groen, A.K.; Venema, K.; Reijngoud, D.J.; Bakker, B.M. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid. Res. 2013, 54, 2325–2340. [Google Scholar] [CrossRef] [Green Version]
- Morrison, D.J.; Preston, T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 2016, 7, 189–200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohland, C.L.; Jobin, C. Microbial Activities and Intestinal Homeostasis: A Delicate Balance between Health and Disease. Cell. Mol. Gastroenterol. Hepatol. 2015, 1, 28–40. [Google Scholar] [CrossRef] [Green Version]
- Belkaid, Y.; Harrison, O.J. Homeostatic Immunity and the Microbiota. Immunity 2017, 46, 562–576. [Google Scholar] [CrossRef] [Green Version]
- Park, J.; Kim, M.; Kang, S.G.; Jannasch, A.H.; Cooper, B.; Patterson, J.; Kim, C.H. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR–S6K pathway. Mucosal Immunol. 2015, 8, 80–93. [Google Scholar] [CrossRef] [Green Version]
- Singh, N.; Gurav, A.; Sivaprakasam, S.; Brady, E.; Padia, R.; Shi, H.; Thangaraju, M.; Prasad, P.D.; Manicassamy, S.; Munn, D.H.; et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014, 40, 128–139. [Google Scholar] [CrossRef] [Green Version]
- Macia, L.; Tan, J.; Vieira, A.T.; Leach, K.; Stanley, D.; Luong, S.; Maruya, M.; McKenzie, C.I.; Hijikata, A.; Wong, C.; et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun. 2015, 6, 6734. [Google Scholar] [CrossRef] [Green Version]
- Kim, M.H.; Kang, S.G.; Park, J.H.; Yanagisawa, M.; Kim, C.H. Short-chain fatty acids activate GPR41 and GPR43 on intestinal epithelial cells to promote inflammatory responses in mice. Gastroenterology 2013, 145, 396–406.e1–10. [Google Scholar] [CrossRef] [PubMed]
- Matthews, G.M.; Howarth, G.S.; Butler, R.N. Short-chain fatty acids induce apoptosis in colon cancer cells associated with changes to intracellular redox state and glucose metabolism. Chemotherapy 2012, 58, 102–109. [Google Scholar] [CrossRef] [PubMed]
- Venegas, D.P.; De la Fuente, M.K.; Landskron, G.; Gonzalez, 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]
- Gustafsson, B.E.; Daft, F.S.; McDaniel, E.G.; Smith, J.C.; Fitzgerald, R.J. Effects of vitamin K-active compounds and intestinal microorganisms in vitamin K-deficient germfree rats. J. Nutr. 1962, 78, 461–468. [Google Scholar] [CrossRef] [PubMed]
- Courtemanche, C.; Elson-Schwab, I.; Mashiyama, S.T.; Kerry, N.; Ames, B.N. Folate deficiency inhibits the proliferation of primary human CD8+ T lymphocytes in vitro. J. Immunol. 2004, 173, 3186–3192. [Google Scholar] [CrossRef] [Green Version]
- Sperandio, V. Take Your Pick: Vitamins and Microbiota Facilitate Pathogen Clearance. Cell Host Microbe 2017, 21, 130–131. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Quan, G.; Jiang, X.; Yang, Y.; Ding, X.; Zhang, D.; Wang, X.; Hardwidge, P.R.; Ren, W.; Zhu, G. Effects of Metabolites Derived from Gut Microbiota and Hosts on Pathogens. Front. Cell. Infect. Microbiol. 2018, 8, 314. [Google Scholar] [CrossRef] [Green Version]
- Connolly, J.P.; Gabrielsen, M.; Goldstone, R.J.; Grinter, R.; Wang, D.; Cogdell, R.J.; Walker, D.; Smith, D.G.; Roe, A.J. A Highly Conserved Bacterial D-Serine Uptake System Links Host Metabolism and Virulence. PLoS Pathog. 2016, 12, e1005359. [Google Scholar] [CrossRef] [Green Version]
- Wells, P.M.; Williams, F.M.K.; Matey-Hernandez, M.L.; Menni, C.; Steves, C.J. ‘RA and the microbiome: Do host genetic factors provide the link? J. Autoimmun. 2019, 99, 104–115. [Google Scholar] [CrossRef]
- Scher, J.U.; Bretz, W.A.; Abramson, S.B. Periodontal disease and subgingival microbiota as contributors for rheumatoid arthritis pathogenesis: Modifiable risk factors? Curr. Opin. Rheumatol. 2014, 26, 424–429. [Google Scholar] [CrossRef] [Green Version]
- Andrews, C.R.; Hoke, M. A preliminary report on the relation of albuminous putrefaction in the intestines to arthritis deformans (rheumatoid arthritis, osteo-arthritis); its influence upon treatment. Am. J. Orthop. Surg. 1907, 2, 61–72. [Google Scholar]
- Kohashi, O.; Kuwata, J.; Umehara, K.; Uemura, F.; Takahashi, T.; Ozawa, A. Susceptibility to adjuvant-induced arthritis among germfree, specific-pathogen-free, and conventional rats. Infect. Immun. 1979, 26, 791–794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Aa, L.X.; Fei, F.; Qi, Q.; Sun, R.B.; Gu, S.H.; Di, Z.Z.; Aa, J.Y.; Wang, G.J.; Liu, C.X. Rebalancing of the gut flora and microbial metabolism is responsible for the anti-arthritis effect of kaempferol. Acta Pharmacol. Sin. 2020, 41, 73–81. [Google Scholar] [CrossRef] [PubMed]
- Round, J.L.; Mazmanian, S.K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2010, 107, 12204–12209. [Google Scholar] [CrossRef] [Green Version]
- Tajik, N.; Frech, M.; Schulz, O.; Schalter, F.; Lucas, S.; Azizov, V.; Durholz, K.; Steffen, F.; Omata, Y.; Rings, A.; et al. Targeting zonulin and intestinal epithelial barrier function to prevent onset of arthritis. Nat. Commun. 2020, 11, 1995. [Google Scholar] [CrossRef] [Green Version]
- Sakaguchi, N.; Takahashi, T.; Hata, H.; Nomura, T.; Tagami, T.; Yamazaki, S.; Sakihama, T.; Matsutani, T.; Negishi, I.; Nakatsuru, 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, 454–460. [Google Scholar] [CrossRef]
- Maeda, Y.; Kurakawa, T.; Umemoto, E.; Motooka, D.; Ito, Y.; Gotoh, K.; Hirota, K.; Matsushita, M.; Furuta, Y.; Narazaki, M.; et al. Dysbiosis Contributes to Arthritis Development via Activation of Autoreactive T Cells in the Intestine. Arthritis Rheumatol. 2016, 68, 2646–2661. [Google Scholar] [CrossRef]
- Monach, P.A.; Mathis, D.; Benoist, C. The K/BxN arthritis model. Curr. Protoc. Immunol. 2008, 81, 15–22. [Google Scholar] [CrossRef]
- Abdollahi-Roodsaz, S.; Joosten, L.A.; Koenders, M.I.; Devesa, I.; Roelofs, M.F.; Radstake, T.R.; Heuvelmans-Jacobs, M.; Akira, S.; Nicklin, M.J.; Ribeiro-Dias, F.; 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, 205–216. [Google Scholar] [CrossRef] [Green Version]
- Chen, B.; Chen, H.; Shu, X.; Yin, Y.; Li, J.; Qin, J.; Chen, L.; Peng, K.; Xu, F.; Gu, W.; et al. Presence of Segmented Filamentous Bacteria in Human Children and Its Potential Role in the Modulation of Human Gut Immunity. Front. Microbiol. 2018, 9, 1403. [Google Scholar] [CrossRef]
- Flak, M.B.; Colas, R.A.; Munoz-Atienza, E.; Curtis, M.A.; Dalli, J.; Pitzalis, C. Inflammatory arthritis disrupts gut resolution mechanisms, promoting barrier breakdown by Porphyromonas gingivalis. JCI Insight 2019, 4, e125191. [Google Scholar] [CrossRef] [PubMed]
- Rogier, R.; Ederveen, T.H.A.; Boekhorst, J.; Wopereis, H.; Scher, J.U.; Manasson, J.; Frambach, S.; Knol, J.; Garssen, J.; van der Kraan, P.M.; et al. Aberrant intestinal microbiota due to IL-1 receptor antagonist deficiency promotes IL-17- and TLR4-dependent arthritis. Microbiome 2017, 5, 63. [Google Scholar] [CrossRef] [PubMed]
- Alunno, A.; Manetti, M.; Caterbi, S.; Ibba-Manneschi, L.; Bistoni, O.; Bartoloni, E.; Valentini, V.; Terenzi, R.; Gerli, R. Altered immunoregulation in rheumatoid arthritis: The role of regulatory T cells and proinflammatory Th17 cells and therapeutic implications. Mediat. Inflamm. 2015, 2015, 751793. [Google Scholar] [CrossRef] [PubMed]
- Yuichi, M.; Takeda, K. Role of Gut Microbiota in Rheumatoid Arthritis. J. Clin. Med. 2017, 6, 60. [Google Scholar]
- Kishikawa, T.; Maeda, Y.; Nii, T.; Motooka, D.; Matsumoto, Y.; Matsushita, M.; Matsuoka, H.; Yoshimura, M.; Kawada, S.; Teshigawara, S.; et al. Metagenome-wide association study of gut microbiome revealed novel aetiology of rheumatoid arthritis in the Japanese population. Ann. Rheum. Dis. 2020, 79, 103–111. [Google Scholar] [CrossRef]
- Tong, Y.; Tang, H.; Li, Y.; Su, L.; Wu, Y.; Bozec, A.; Zaiss, M.; Qing, P.; Zhao, H.; Tan, C.; et al. Gut Microbiota Dysbiosis in High-Risk Individuals for Rheumatoid Arthritis Triggers Mucosal Immunity Perturbation and Promotes Arthritis in Mice. Res. Sq. 2020. [Google Scholar] [CrossRef]
- Alpizar-Rodriguez, D.; Lesker, T.R.; Gronow, A.; Gilbert, B.; Raemy, E.; Lamacchia, C.; Gabay, C.; Finckh, A.; Strowig, T. Prevotella copri in individuals at risk for rheumatoid arthritis. Ann. Rheum. Dis. 2019, 78, 590–593. [Google Scholar] [CrossRef]
- Scher, J.U.; Sczesnak, A.; Longman, R.S.; Segata, N.; Ubeda, C.; Bielski, C.; Rostron, T.; Cerundolo, V.; Pamer, E.G.; Abramson, S.B.; et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2013, 2, e01202. [Google Scholar] [CrossRef]
- Han, M.; Zhang, N.; Mao, Y.; Huang, B.; Ren, M.; Peng, Z.; Bai, Z.; Chen, L.; Liu, Y.; Wang, S.; et al. The Potential of Gut Microbiota Metabolic Capability to Detect Drug Response in Rheumatoid Arthritis Patients. Front. Microbiol. 2022, 13, 839015. [Google Scholar] [CrossRef]
- Pianta, A.; Arvikar, S.; Strle, K.; Drouin, E.E.; Wang, Q.; Costello, C.E.; Steere, A.C. Evidence of the Immune Relevance of Prevotella copri, a Gut Microbe, in Patients with Rheumatoid Arthritis. Arthritis Rheumatol. 2017, 69, 964–975. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Wright, K.; Davis, J.M.; Jeraldo, P.; Marietta, E.V.; Murray, J.; Nelson, H.; Matteson, E.L.; Taneja, V. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med. 2016, 8, 43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cordain, L.; Eaton, S.B.; Sebastian, A.; Mann, N.; Lindeberg, S.; Watkins, B.A.; O’Keefe, J.H.; Brand-Miller, J. Origins and evolution of the Western diet: Health implications for the 21st century. Am. J. Clin. Nutr. 2005, 81, 341–354. [Google Scholar] [CrossRef] [PubMed]
- Smits, S.A.; Leach, J.; Sonnenburg, E.D.; Gonzalez, C.G.; Lichtman, J.S.; Reid, G.; Knight, R.; Manjurano, A.; Changalucha, J.; Elias, J.E.; et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 2017, 357, 802–806. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ghosh, T.S.; Rampelli, S.; Jeffery, I.B.; Santoro, A.; Neto, M.; Capri, M.; Giampieri, E.; Jennings, A.; Candela, M.; Turroni, S.; et al. Mediterranean diet intervention alters the gut microbiome in older people reducing frailty and improving health status: The NU-AGE 1-year dietary intervention across five European countries. Gut 2020, 69, 1218–1228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rinott, E.; Meir, A.Y.; Tsaban, G.; Zelicha, H.; Kaplan, A.; Knights, D.; Tuohy, K.; Scholz, M.U.; Koren, O.; Stampfer, M.J.; et al. The effects of the Green-Mediterranean diet on cardiometabolic health are linked to gut microbiome modifications: A randomized controlled trial. Genome Med. 2022, 14, 29. [Google Scholar] [CrossRef]
- Nagpal, R.; Shively, C.A.; Register, T.C.; Craft, S.; Yadav, H. Gut microbiome-Mediterranean diet interactions in improving host health. F1000Res 2019, 8, 699. [Google Scholar] [CrossRef] [Green Version]
- Tsigalou, C.; Paraschaki, A.; Karvelas, A.; Kantartzi, K.; Gagali, K.; Tsairidis, D.; Bezirtzoglou, E. Gut microbiome and Mediterranean diet in the context of obesity. Current knowledge, perspectives and potential therapeutic targets. Metab. Open 2021, 9, 100081. [Google Scholar] [CrossRef]
- Meslier, V.; Laiola, M.; Roager, H.M.; De Filippis, F.; Roume, H.; Quinquis, B.; Giacco, R.; Mennella, I.; Ferracane, R.; Pons, N.; et al. Mediterranean diet intervention in overweight and obese subjects lowers plasma cholesterol and causes changes in the gut microbiome and metabolome independently of energy intake. Gut 2020, 69, 1258–1268. [Google Scholar] [CrossRef] [Green Version]
- Gutierrez-Diaz, I.; Fernandez-Navarro, T.; Sanchez, B.; Margolles, A.; Gonzalez, S. Mediterranean diet and faecal microbiota: A transversal study. Food Funct. 2016, 7, 2347–2356. [Google Scholar] [CrossRef]
- So, D.; Whelan, K.; Rossi, M.; Morrison, M.; Holtmann, G.; Kelly, J.T.; Shanahan, E.R.; Staudacher, H.M.; Campbell, K.L. Dietary fiber intervention on gut microbiota composition in healthy adults: A systematic review and meta-analysis. Am. J. Clin. Nutr. 2018, 107, 965–983. [Google Scholar] [CrossRef] [Green Version]
- Philippou, E.; Nikiphorou, E. Are we really what we eat? Nutrition and its role in the onset of rheumatoid arthritis. Autoimmun. Rev. 2018, 17, 1074–1077. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Santangelo, C.; Vari, R.; Scazzocchio, B.; De Sanctis, P.; Giovannini, C.; D’Archivio, M.; Masella, R. Anti-inflammatory Activity of Extra Virgin Olive Oil Polyphenols: Which Role in the Prevention and Treatment of Immune-Mediated Inflammatory Diseases? Endocr. Metab. Immune Disord. Drug Targets 2018, 18, 36–50. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, S.; Whitley, C.S.; Haribabu, B.; Jala, V.R. Regulation of Intestinal Barrier Function by Microbial Metabolites. Cell. Mol. Gastroenterol. Hepatol. 2021, 11, 1463–1482. [Google Scholar] [CrossRef] [PubMed]
- Sundqvist, T.; Lindstrom, F.; Magnusson, K.E.; Skoldstam, L.; Stjernstrom, I.; Tagesson, C. Influence of fasting on intestinal permeability and disease activity in patients with rheumatoid arthritis. Scand. J. Rheumatol. 1982, 11, 33–38. [Google Scholar] [CrossRef]
- Skoldstam, L.; Larsson, L.; Lindstrom, F.D. Effect of fasting and lactovegetarian diet on rheumatoid arthritis. Scand. J. Rheumatol. 1979, 8, 249–255. [Google Scholar] [CrossRef]
- Kjeldsen-Kragh, J.; Haugen, M.; Borchgrevink, C.F.; Laerum, E.; Eek, M.; Mowinkel, P.; Hovi, K.; Forre, O. Controlled trial of fasting and one-year vegetarian diet in rheumatoid arthritis. Lancet 1991, 338, 899–902. [Google Scholar] [CrossRef]
- Scaioli, E.; Liverani, E.; Belluzzi, A. The Imbalance between n-6/n-3 Polyunsaturated Fatty Acids and Inflammatory Bowel Disease: A Comprehensive Review and Future Therapeutic Perspectives. Int. J. Mol. Sci. 2017, 18, 2619. [Google Scholar] [CrossRef] [Green Version]
- Podas, T.; Nightingale, J.M.; Oldham, R.; Roy, S.; Sheehan, N.J.; Mayberry, J.F. Is rheumatoid arthritis a disease that starts in the intestine? A pilot study comparing an elemental diet with oral prednisolone. Postgrad. Med. J. 2007, 83, 128–131. [Google Scholar] [CrossRef] [Green Version]
- Durholz, K.; Hofmann, J.; Iljazovic, A.; Hager, J.; Lucas, S.; Sarter, K.; Strowig, T.; Bang, H.; Rech, J.; Schett, G.; et al. Dietary Short-Term Fiber Interventions in Arthritis Patients Increase Systemic SCFA Levels and Regulate Inflammation. Nutrients 2020, 12, 3207. [Google Scholar] [CrossRef]
- Jonsson, I.M.; Verdrengh, M.; Brisslert, M.; Lindblad, S.; Bokarewa, M.; Islander, U.; Carlsten, H.; Ohlsson, C.; Nandakumar, K.S.; Holmdahl, R.; et al. Ethanol prevents development of destructive arthritis. Proc. Natl. Acad. Sci. USA 2007, 104, 258–263. [Google Scholar] [CrossRef] [Green Version]
- Kallberg, H.; Jacobsen, S.; Bengtsson, C.; Pedersen, M.; Padyukov, L.; Garred, P.; Frisch, M.; Karlson, E.W.; Klareskog, L.; Alfredsson, L. Alcohol consumption is associated with decreased risk of rheumatoid arthritis: Results from two Scandinavian case-control studies. Ann. Rheum. Dis. 2009, 68, 222–227. [Google Scholar] [CrossRef] [PubMed]
- Mikuls, T.R.; Cerhan, J.R.; Criswell, L.A.; Merlino, L.; Mudano, A.S.; Burma, M.; Folsom, A.R.; Saag, K.G. Coffee, tea, and caffeine consumption and risk of rheumatoid arthritis: Results from the Iowa Women’s Health Study. Arthritis Rheum. 2002, 46, 83–91. [Google Scholar] [CrossRef]
- Sundström, B.; Johansson, I.; Rantapää-Dahlqvist, S. Interaction between dietary sodium and smoking increases the risk for rheumatoid arthritis: Results from a nested case-control study. Rheumatology 2015, 54, 487–493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alpízar-Rodríguez, D.; Finckh, A.; Gilbert, B. The Role of Nutritional Factors and Intestinal Microbiota in Rheumatoid Arthritis Development. Nutrients 2020, 13, 96. [Google Scholar] [CrossRef] [PubMed]
- Bae, J.H.; Shin, M.Y.; Kang, E.H.; Lee, Y.J.; Ha, Y.J. Association of rheumatoid arthritis and high sodium intake with major adverse cardiovascular events: A cross-sectional study from the seventh Korean National Health and Nutrition Examination Survey. BMJ Open 2021, 11, e056255. [Google Scholar] [CrossRef]
- Choi, H.H.; Cho, Y.S. Fecal Microbiota Transplantation: Current Applications, Effectiveness, and Future Perspectives. Clin. Endosc. 2016, 49, 257–265. [Google Scholar] [CrossRef]
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [Google Scholar] [CrossRef] [Green Version]
- Bungau, S.G.; Behl, T.; Singh, A.; Sehgal, A.; Singh, S.; Chigurupati, S.; Vijayabalan, S.; Das, S.; Palanimuthu, V.R. Targeting Probiotics in Rheumatoid Arthritis. Nutrients 2021, 13, 3376. [Google Scholar] [CrossRef]
- Kato, I.; Endo-Tanaka, K.; Yokokura, T. Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci. 1998, 63, 635–644. [Google Scholar] [CrossRef]
- Fan, Z.; Yang, B.; Ross, R.P.; Stanton, C.; Shi, G.; Zhao, J.; Zhang, H.; Chen, W. Protective effects of Bifidobacterium adolescentis on collagen-induced arthritis in rats depend on timing of administration. Food Funct. 2020, 11, 4499–4511. [Google Scholar] [CrossRef]
- Yamashita, M.; Matsumoto, K.; Endo, T.; Ukibe, K.; Hosoya, T.; Matsubara, Y.; Nakagawa, H.; Sakai, F.; Miyazaki, T. Preventive Effect of Lactobacillus helveticus SBT2171 on Collagen-Induced Arthritis in Mice. Front. Microbiol. 2017, 8, 1159. [Google Scholar] [CrossRef]
- Hatakka, K.; Martio, J.; Korpela, M.; Herranen, M.; Poussa, T.; Laasanen, T.; Saxelin, M.; Vapaatalo, H.; Moilanen, E.; Korpela, R. Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis—A pilot study. Scand. J. Rheumatol. 2003, 32, 211–215. [Google Scholar] [CrossRef] [PubMed]
- Vaghef-Mehrabany, E.; Alipour, B.; Homayouni-Rad, A.; Sharif, S.K.; Asghari-Jafarabadi, M.; Zavvari, S. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis. Nutrition 2014, 30, 430–435. [Google Scholar] [CrossRef] [PubMed]
- Alipour, B.; Homayouni-Rad, A.; Vaghef-Mehrabany, E.; Sharif, S.K.; Vaghef-Mehrabany, L.; Asghari-Jafarabadi, M.; Nakhjavani, M.R.; Mohtadi-Nia, J. 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. [Google Scholar]
- Cannarella, L.A.T.; Mari, N.L.; Alcantara, C.C.; Iryioda, T.M.V.; Costa, N.T.; Oliveira, S.R.; Lozovoy, M.A.B.; Reiche, E.M.V.; Dichi, I.; Simao, A.N.C. Mixture of probiotics reduces inflammatory biomarkers and improves the oxidative/nitrosative profile in people with rheumatoid arthritis. Nutrition 2021, 89, 111282. [Google Scholar] [CrossRef] [PubMed]
- Dimidi, E.; Cox, S.R.; Rossi, M.; Whelan, K. Fermented Foods: Definitions and Characteristics, Impact on the Gut Microbiota and Effects on Gastrointestinal Health and Disease. Nutrients 2019, 11, 1806. [Google Scholar] [CrossRef] [Green Version]
- Fijan, S. Microorganisms with claimed probiotic properties: An overview of recent literature. Int. J. Environ. Res. Public Health 2014, 11, 4745–4767. [Google Scholar] [CrossRef]
- Terpou, A.; Papadaki, A.; Lappa, I.K.; Kachrimanidou, V.; Bosnea, L.A.; Kopsahelis, N. Probiotics in Food Systems: Significance and Emerging Strategies Towards Improved Viability and Delivery of Enhanced Beneficial Value. Nutrients 2019, 11, 1591. [Google Scholar] [CrossRef] [Green Version]
- Pena-Rodriguez, M.; Vega-Magana, N.; Garcia-Benavides, L.; Zepeda-Nuno, J.S.; Gutierrez-Silerio, G.Y.; Gonzalez-Hernandez, L.A.; Andrade-Villanueva, J.F.; Del Toro-Arreola, S.; Pereira-Suarez, A.L.; Bueno-Topete, M.R. Butyrate administration strengthens the intestinal epithelium and improves intestinal dysbiosis in a cholestasis fibrosis model. J. Appl. Microbiol. 2022, 132, 571–583. [Google Scholar] [CrossRef]
- Zhang, Q.; Li, Y.; Chen, L. Effect of berberine in treating type 2 diabetes mellitus and complications and its relevant mechanisms. Zhongguo Zhong Yao Za Zhi 2015, 40, 1660–1665. [Google Scholar]
- Abdill, R.J.; Adamowicz, E.M.; Blekhman, R. Public human microbiome data are dominated by highly developed countries. PLoS Biol. 2022, 20, e3001536. [Google Scholar] [CrossRef] [PubMed]
- Bakshi, A.M. Gene patents at the Supreme Court: Association for Molecular Pathology v. Myriad Genetics. J. Law Biosci. 2014, 1, 183–189. [Google Scholar] [CrossRef] [PubMed]
Phylum | Class | Order |
---|---|---|
Firmicutes | Clostridia | Clostridiales |
Bacilli | Lactobacillales | |
Erysipheoltrichia | Erisophelotrichales | |
Negativicutes | Selenomonadales | |
Veillonellales | ||
Bacteroidetes | Bacteroidia | Bacteroidales |
Actinobacteria | Coriobacteria | Coriobacteriales |
Eggerthellales | ||
Actinobacteria | Bifidobacteriales | |
Fusobacteria | Fusobacteria | Fusobacteriales |
Proteobacteria | Gammaproteobacteria | Enterobacteriales |
Aeromonadales |
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
Attur, M.; Scher, J.U.; Abramson, S.B.; Attur, M. Role of Intestinal Dysbiosis and Nutrition in Rheumatoid Arthritis. Cells 2022, 11, 2436. https://doi.org/10.3390/cells11152436
Attur M, Scher JU, Abramson SB, Attur M. Role of Intestinal Dysbiosis and Nutrition in Rheumatoid Arthritis. Cells. 2022; 11(15):2436. https://doi.org/10.3390/cells11152436
Chicago/Turabian StyleAttur, Malavikalakshmi, Jose U Scher, Steven B. Abramson, and Mukundan Attur. 2022. "Role of Intestinal Dysbiosis and Nutrition in Rheumatoid Arthritis" Cells 11, no. 15: 2436. https://doi.org/10.3390/cells11152436
APA StyleAttur, M., Scher, J. U., Abramson, S. B., & Attur, M. (2022). Role of Intestinal Dysbiosis and Nutrition in Rheumatoid Arthritis. Cells, 11(15), 2436. https://doi.org/10.3390/cells11152436