#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Molecular characterisation of the synovial fluid microbiome in rheumatoid arthritis patients and healthy control subjects


Autoři: Dargham Bayan Mohsen Hammad aff001;  Veranja Liyanapathirana aff002;  Daniel Paul Tonge aff001
Působiště autorů: School of Life Sciences, Faculty of Natural Sciences, Keele University, Keele, Newcastle, England, United Kingdom aff001;  Department of Microbiology, Faculty of Medicine, University of Peradeniya, Kandy, Sri Lanka aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225110

Souhrn

The colonisation of specific body sites in contact with the external environment by microorganisms is both well-described and universally accepted, whereas, the existence of microbial evidence in other “classically sterile” locations including the blood, synovial space, and lungs, is a relatively new concept. Increasingly, a role for the microbiome in disease is being considered, and it is therefore necessary to increase our understanding of these. To date, little data support the existence of a “synovial fluid microbiome”.

Methods

The presence and identity of bacterial and fungal DNA in the synovial fluid of rheumatoid arthritis (RA) patients and healthy control subjects was investigated through amplification and sequencing of the bacterial 16S rRNA gene and fungal internal transcribed spacer region 2 respectively. Synovial fluid concentrations of the cytokines IL-6, IL-17A, IL22 and IL-23 were determined by ELISA.

Results

Bacterial 16S rRNA genes were detected in 87.5% RA patients, and all healthy control subjects. At the phylum level, the microbiome was predominated by Proteobacteria (Control = 83.5%, RA = 79.3%) and Firmicutes (Control = 16.1%, RA = 20.3%), and to a much lesser extent, Actinobacteria (Control = 0.2%, RA = 0.3%) and Bacteroidetes (Control = 0.1%, RA = 0.1%). Fungal DNA was identified in 75% RA samples, and 88.8% healthy controls. At the phylum level, synovial fluid was predominated by members of the Basidiomycota (Control = 53.9%, RA = 46.9%) and Ascomycota (Control = 35.1%, RA = 50.8%) phyla. Statistical analysis revealed key taxa that were differentially present or abundant dependent on disease status.

Conclusions

This study reports the presence of a synovial fluid microbiome, and determines that this is modulated by disease status (RA) as are other classical microbiome niches.

Klíčová slova:

Bacteria – Fungal genetics – Gene sequencing – Microbiome – Polymerase chain reaction – Rheumatoid arthritis – Ribosomal RNA – Synovial fluid


Zdroje

1. Marchesi JR, Ravel J. The vocabulary of microbiome research: a proposal. Microbiome. 2015;3:31. Epub 2015/07/30. doi: 10.1186/s40168-015-0094-5 26229597.

2. Sender R, Fuchs S, Milo R. Revised Estimates for the Number of Human and Bacteria Cells in the Body. PLoS Biol. 2016;14(8):e1002533. Epub 2016/08/19. doi: 10.1371/journal.pbio.1002533 27541692.

3. Markova ND. L-form bacteria cohabitants in human blood: significance for health and diseases. Discov Med. 2017;23(128):305–13. 28715646.

4. Whittle E, Leonard M, Harrison R, Gant T, Tonge D. Multi-Method Characterisation of the Human Circulating Microbiome. BioRxiv. 2018. Epub 2018. https://doi.org/10.1101/359760.

5. Zhao Y, Chen B, Li S, Yang L, Zhu D, Wang Y, et al. Detection and characterization of bacterial nucleic acids in culture-negative synovial tissue and fluid samples from rheumatoid arthritis or osteoarthritis patients. Sci Rep. 2018;8(1):14305. Epub 2018/09/24. doi: 10.1038/s41598-018-32675-w 30250232.

6. Mao Q, Jiang F, Yin R, Wang J, Xia W, Dong G, et al. Interplay between the lung microbiome and lung cancer. Cancer Lett. 2018;415:40–8. Epub 2017/12/02. doi: 10.1016/j.canlet.2017.11.036 29197615.

7. Moffatt MF, Cookson WO. The lung microbiome in health and disease. Clin Med (Lond). 2017;17(6):525–9. doi: 10.7861/clinmedicine.17-6-525 29196353.

8. O’Dwyer DN, Dickson RP, Moore BB. The Lung Microbiome, Immunity, and the Pathogenesis of Chronic Lung Disease. J Immunol. 2016;196(12):4839–47. doi: 10.4049/jimmunol.1600279 27260767.

9. Wang L, Hao K, Yang T, Wang C. Role of the Lung Microbiome in the Pathogenesis of Chronic Obstructive Pulmonary Disease. Chin Med J (Engl). 2017;130(17):2107–11. doi: 10.4103/0366-6999.211452 28741603.

10. Gibofsky A. Overview of epidemiology, pathophysiology, and diagnosis of rheumatoid arthritis. Am J Manag Care. 2012;18(13 Suppl):S295–302. 23327517.

11. Pretorius E, Akeredolu OO, Soma P, Kell DB. Major involvement of bacterial components in rheumatoid arthritis and its accompanying oxidative stress, systemic inflammation and hypercoagulability. Exp Biol Med (Maywood). 2017;242(4):355–73. Epub 2016/11/26. doi: 10.1177/1535370216681549 27889698.

12. 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(8):895–905. Epub 2015/07/27. doi: 10.1038/nm.3914 26214836.

13. Lopez-Oliva I, Paropkari AD, Saraswat S, Serban S, Yonel Z, Sharma P, et al. Dysbiotic Subgingival Microbial Communities in Periodontally Healthy Patients With Rheumatoid Arthritis. Arthritis Rheumatol. 2018;70(7):1008–13. Epub 2018/05/21. doi: 10.1002/art.40485 29513935.

14. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife. 2013;2:e01202. doi: 10.7554/eLife.01202 24192039.

15. Taneja V. Arthritis susceptibility and the gut microbiome. FEBS Lett. 2014;588(22):4244–9. doi: 10.1016/j.febslet.2014.05.034 24873878.

16. Chen J, Wright K, Davis JM, Jeraldo P, Marietta EV, Murray J, et al. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis. Genome Med. 2016;8(1):43. Epub 2016/04/21. doi: 10.1186/s13073-016-0299-7 27102666.

17. Liu X, Zeng B, Zhang J, Li W, Mou F, Wang H, et al. Role of the Gut Microbiome in Modulating Arthritis Progression in Mice. Sci Rep. 2016;6:30594. doi: 10.1038/srep30594 27481047.

18. Scher JU, Littman DR, Abramson SB. Microbiome in Inflammatory Arthritis and Human Rheumatic Diseases. Arthritis Rheumatol. 2016;68(1):35–45. doi: 10.1002/art.39259 26331579.

19. 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. doi: 10.1002/art.39783 27333153.

20. Vaahtovuo J, Munukka E, Korkeamäki M, Luukkainen R, Toivanen P. Fecal microbiota in early rheumatoid arthritis. J Rheumatol. 2008;35(8):1500–5. Epub 2008/06/01. 18528968.

21. Liu X, Zou Q, Zeng B, Fang Y, Wei H. Analysis of fecal Lactobacillus community structure in patients with early rheumatoid arthritis. Curr Microbiol. 2013;67(2):170–6. Epub 2013/03/13. doi: 10.1007/s00284-013-0338-1 23483307.

22. Wu X, Liu J, Xiao L, Lu A, Zhang G. Alterations of Gut Microbiome in Rheumatoid Arthritis. Osteoarthritis and Cartilage. 2017;25:S287–S8.

23. Brusca SB, Abramson SB, Scher JU. Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity. Curr Opin Rheumatol. 2014;26(1):101–7. doi: 10.1097/BOR.0000000000000008 24247114.

24. Demoruelle MK, Solomon JJ, Fischer A, Deane KD. The lung may play a role in the pathogenesis of rheumatoid arthritis. Int J Clin Rheumtol. 2014;9(3):295–309 26089988.

25. Scher JU, Joshua V, Artacho A, Abdollahi-Roodsaz S, Öckinger J, Kullberg S, et al. The lung microbiota in early rheumatoid arthritis and autoimmunity. Microbiome. 2016;4(1):60. Epub 2016/11/17. doi: 10.1186/s40168-016-0206-x 27855721.

26. Ebringer A, Rashid T. Rheumatoid arthritis is an autoimmune disease triggered by Proteus urinary tract infection. Clin Dev Immunol. 2006;13(1):41–8. doi: 10.1080/17402520600576578 16603443.

27. Ebringer A, Rashid T. Rheumatoid arthritis is caused by a Proteus urinary tract infection. APMIS. 2014;122(5):363–8. Epub 2013/08/29. doi: 10.1111/apm.12154 23992372.

28. Tani Y, Tiwana H, Hukuda S, Nishioka J, Fielder M, Wilson C, et al. Antibodies to Klebsiella, Proteus, and HLA-B27 peptides in Japanese patients with ankylosing spondylitis and rheumatoid arthritis. J Rheumatol. 1997;24(1):109–14. 9002020.

29. Wilson C, Thakore A, Isenberg D, Ebringer A. Correlation between anti-Proteus antibodies and isolation rates of P. mirabilis in rheumatoid arthritis. Rheumatol Int. 1997;16(5):187–9. doi: 10.1007/bf01330294 9032817.

30. Chi H, Flavell RA. Innate recognition of non-self nucleic acids. Genome Biol. 2008;9(3):211. Epub 2008/03/10. doi: 10.1186/gb-2008-9-3-211 18341708.

31. Atianand MK, Fitzgerald KA. Molecular basis of DNA recognition in the immune system. J Immunol. 2013;190(5):1911–8. doi: 10.4049/jimmunol.1203162 23417527.

32. Castañeda-Delgado JE, Bastián-Hernandez Y, Macias-Segura N, Santiago-Algarra D, Castillo-Ortiz JD, Alemán-Navarro AL, et al. Type I Interferon Gene Response Is Increased in Early and Established Rheumatoid Arthritis and Correlates with Autoantibody Production. Front Immunol. 2017;8:285. Epub 2017/03/20. doi: 10.3389/fimmu.2017.00285 28373872.

33. Enninga EA, Nevala WK, Holtan SG, Markovic SN. Immune Reactivation by Cell-Free Fetal DNA in Healthy Pregnancies Re-Purposed to Target Tumors: Novel Checkpoint Inhibition in Cancer Therapeutics. Front Immunol. 2015;6:424. Epub 2015/08/26. doi: 10.3389/fimmu.2015.00424 26379664.

34. Rossol M, Heine H, Meusch U, Quandt D, Klein C, Sweet MJ, et al. LPS-induced cytokine production in human monocytes and macrophages. Crit Rev Immunol. 2011;31(5):379–446. 22142165.

35. Ross JJ. Septic Arthritis of Native Joints. Infect Dis Clin North Am. 2017;31(2):203–18. Epub 2017/03/30. doi: 10.1016/j.idc.2017.01.001 28366221.

36. Martinez-Martinez RE, Abud-Mendoza C, Patiño-Marin N, Rizo-Rodríguez JC, Little JW, Loyola-Rodríguez JP. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol. 2009;36(12):1004–10. doi: 10.1111/j.1600-051X.2009.01496.x 19929953.

37. Moen K, Brun JG, Valen M, Skartveit L, Eribe EK, Olsen I, et al. Synovial inflammation in active rheumatoid arthritis and psoriatic arthritis facilitates trapping of a variety of oral bacterial DNAs. Clin Exp Rheumatol. 2006;24(6):656–63. 17207381.

38. Ogrendik M. Rheumatoid arthritis is linked to oral bacteria: etiological association. Modern rheumatology. 2009;19(5):453–6. doi: 10.1007/s10165-009-0194-9 19554393

39. Reichert S, Haffner M, Keyßer G, Schäfer C, Stein JM, Schaller HG, et al. Detection of oral bacterial DNA in synovial fluid. Journal of clinical periodontology. 2013;40(6):591–8. doi: 10.1111/jcpe.12102 23534379

40. Témoin S, Chakaki A, Askari A, El-Halaby A, Fitzgerald S, Marcus RE, et al. Identification of oral bacterial DNA in synovial fluid of arthritis patients with native and failed prosthetic joints. Journal of clinical rheumatology: practical reports on rheumatic & musculoskeletal diseases. 2012;18(3):117.

41. Gérard HC, Wang Z, Wang GF, El-Gabalawy H, Goldbach-Mansky R, Li Y, et al. Chromosomal DNA from a variety of bacterial species is present in synovial tissue from patients with various forms of arthritis. Arthritis Rheum. 2001;44(7):1689–97. doi: 10.1002/1529-0131(200107)44:7<1689::AID-ART293>3.0.CO;2-K 11465721.

42. Kempsell KE, Cox CJ, Hurle M, Wong A, Wilkie S, Zanders ED, et al. Reverse transcriptase-PCR analysis of bacterial rRNA for detection and characterization of bacterial species in arthritis synovial tissue. Infect Immun. 2000;68(10):6012–26. doi: 10.1128/iai.68.10.6012-6026.2000 10992514.

43. Hitchon CA, Chandad F, Ferucci ED, Willemze A, Ioan-Facsinay A, van der Woude D, et al. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol. 2010;37(6):1105–12. Epub 2010/05/01. doi: 10.3899/jrheum.091323 20436074.

44. Lundberg K, Kinloch A, Fisher BA, Wegner N, Wait R, Charles P, et al. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 2008;58(10):3009–19. doi: 10.1002/art.23936 18821669.

45. Ogrendik M, Kokino S, Ozdemir F, Bird PS, Hamlet S. Serum antibodies to oral anaerobic bacteria in patients with rheumatoid arthritis. MedGenMed. 2005;7(2):2. Epub 2005/06/16. 16369381.

46. Moen K, Brun JG, Madland TM, Tynning T, Jonsson R. Immunoglobulin G and A antibody responses to Bacteroides forsythus and Prevotella intermedia in sera and synovial fluids of arthritis patients. Clin Diagn Lab Immunol. 2003;10(6):1043–50. doi: 10.1128/CDLI.10.6.1043-1050.2003 14607865.

47. Bartold PM, Marshall RI, Haynes DR. Periodontitis and Rheumatoid Arthritis: A Review. J Periodontol. 2005;76 Suppl 11S:2066–74. doi: 10.1902/jop.2005.76.11-S.2066 29539040.

48. Chen HH, Huang N, Chen YM, Chen TJ, Chou P, Lee YL, et al. Association between a history of periodontitis and the risk of rheumatoid arthritis: a nationwide, population-based, case-control study. Ann Rheum Dis. 2013;72(7):1206–11. Epub 2012/08/31. doi: 10.1136/annrheumdis-2012-201593 22941768.

49. de Pablo P, Dietrich T, McAlindon TE. Association of periodontal disease and tooth loss with rheumatoid arthritis in the US population. J Rheumatol. 2008;35(1):70–6. Epub 2007/11/15. 18050377.

50. Forner L, Larsen T, Kilian M, Holmstrup P. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J Clin Periodontol. 2006;33(6):401–7. doi: 10.1111/j.1600-051X.2006.00924.x 16677328.

51. Horliana AC, Chambrone L, Foz AM, Artese HP, Rabelo MeS, Pannuti CM, et al. Dissemination of periodontal pathogens in the bloodstream after periodontal procedures: a systematic review. PLoS One. 2014;9(5):e98271. Epub 2014/05/28. doi: 10.1371/journal.pone.0098271 24870125.

52. Koziel J, Mydel P, Potempa J. The link between periodontal disease and rheumatoid arthritis: an updated review. Curr Rheumatol Rep. 2014;16(3):408. doi: 10.1007/s11926-014-0408-9 24458478.

53. Ortiz P, Bissada NF, Palomo L, Han YW, Al-Zahrani MS, Panneerselvam A, et al. Periodontal therapy reduces the severity of active rheumatoid arthritis in patients treated with or without tumor necrosis factor inhibitors. J Periodontol. 2009;80(4):535–40. doi: 10.1902/jop.2009.080447 19335072.

54. Scher JU, Ubeda C, Equinda M, Khanin R, Buischi Y, Viale A, et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis. Arthritis Rheum. 2012;64(10):3083–94. doi: 10.1002/art.34539 22576262.

55. Zhao X, Liu Z, Shu D, Xiong Y, He M, Xu S, et al. Association of Periodontitis with Rheumatoid Arthritis and the Effect of Non-Surgical Periodontal Treatment on Disease Activity in Patients with Rheumatoid Arthritis. Med Sci Monit. 2018;24:5802–10. Epub 2018/08/20. doi: 10.12659/MSM.909117 30124222.

56. Li R, Tian C, Postlethwaite A, Jiao Y, Garcia-Godoy F, Pattanaik D, et al. Rheumatoid arthritis and periodontal disease: What are the similarities and differences? Int J Rheum Dis. 2017;20(12):1887–901. Epub 2018/01/09. doi: 10.1111/1756-185X.13240 29341486.

57. Cheng Z, Meade J, Mankia K, Emery P, Devine DA. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31(1):19–30. Epub 2017/09/01. doi: 10.1016/j.berh.2017.08.001 29221594.

58. Potempa J, Mydel P, Koziel J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13(10):606–20. Epub 2017/08/24. doi: 10.1038/nrrheum.2017.132 28835673.

59. Whittle E, Leonard MO, Harrison R, Gant TW, Tonge DP. Multi-Method Characterization of the Human Circulating Microbiome. Frontiers in Microbiology. 2019;9(3266). doi: 10.3389/fmicb.2018.03266 30705670

60. Olsen-Bergem H, Kristoffersen AK, Bjørnland T, Reseland JE, Aas JA. Juvenile idiopathic arthritis and rheumatoid arthritis: bacterial diversity in temporomandibular joint synovial fluid in comparison with immunological and clinical findings. Int J Oral Maxillofac Surg. 2016;45(3):318–22. Epub 2015/11/06. doi: 10.1016/j.ijom.2015.08.986 26554824.

61. Bonnet E, Julia F, Giordano G, Lourtet-Hascoet J. Joint infection due to Raoultella planticola: first report. Infection. 2017;45(5):703–4. Epub 2017/03/23. doi: 10.1007/s15010-017-1006-3 28337666.

62. Levorova J, Machon V, Guha A, Foltan R. Septic arthritis of the temporomandibular joint caused by rare bacteria Raoultella ornithinolytica. Int J Oral Maxillofac Surg. 2017;46(1):111–5. Epub 2016/10/07. doi: 10.1016/j.ijom.2016.09.008 27726907.

63. Venus K, Vaithilingam S, Bogoch II. Septic arthritis of the knee due to Raoultella ornithinolytica. Infection. 2016;44(5):691–2. Epub 2016/08/03. doi: 10.1007/s15010-016-0930-y 27488819.

64. Kanki M, Yoda T, Tsukamoto T, Shibata T. Klebsiella pneumoniae produces no histamine: Raoultella planticola and Raoultella ornithinolytica strains are histamine producers. Appl Environ Microbiol. 2002;68(7):3462–6. doi: 10.1128/AEM.68.7.3462-3466.2002 12089029.

65. Kim KW, Kim BM, Lee KA, Lee SH, Firestein GS, Kim HR. Histamine and Histamine H4 Receptor Promotes Osteoclastogenesis in Rheumatoid Arthritis. Sci Rep. 2017;7(1):1197. Epub 2017/04/26. doi: 10.1038/s41598-017-01101-y 28446753.

66. Peters BA, Wu J, Hayes RB, Ahn J. The oral fungal mycobiome: characteristics and relation to periodontitis in a pilot study. BMC Microbiol. 2017;17(1):157. Epub 2017/07/12. doi: 10.1186/s12866-017-1064-9 28701186.

67. Beatty M, Guduric-Fuchs J, Brown E, Bridgett S, Chakravarthy U, Hogg RE, et al. Small RNAs from plants, bacteria and fungi within the order Hypocreales are ubiquitous in human plasma. BMC Genomics. 2014;15:933. Epub 2014/10/25. doi: 10.1186/1471-2164-15-933 25344700.

68. Hallen-Adams HE, Suhr MJ. Fungi in the healthy human gastrointestinal tract. Virulence. 2017;8(3):352–8. Epub 2016/10/13. doi: 10.1080/21505594.2016.1247140 27736307.

69. Singh H, Joshi P, Khanna V, Gupta SG, Arora S, Maurya V. Pulmonary Aspergilloma in Rheumatoid Arthritis. Med J Armed Forces India. 2003;59(3):254–6. Epub 2011/07/21. doi: 10.1016/S0377-1237(03)80024-2 27407532.

70. Horie M, Tamiya H, Goto Y, Suzuki M, Matsuzaki H, Hasegawa WT, et al. Nonspecific elevation of serum Aspergillus galactomannan antigen levels in patients with rheumatoid arthritis. Respir Investig. 2016;54(1):44–9. Epub 2015/09/26. doi: 10.1016/j.resinv.2015.08.002 26718144.

71. Sandoval-Denis M, Sutton DA, Martin-Vicente A, Cano-Lira JF, Wiederhold N, Guarro J, et al. Cladosporium Species Recovered from Clinical Samples in the United States. J Clin Microbiol. 2015;53(9):2990–3000. Epub 2015/07/15. doi: 10.1128/JCM.01482-15 26179305.

72. Jahreis S, Kuhn S, Madaj AM, Bauer M, Polte T. Mold metabolites drive rheumatoid arthritis in mice via promotion of IFN-gamma- and IL-17-producing T cells. Food Chem Toxicol. 2017;109(Pt 1):405–13. Epub 2017/09/19. doi: 10.1016/j.fct.2017.09.027 28935500.

73. van Hamburg JP, Tas SW. Molecular mechanisms underpinning T helper 17 cell heterogeneity and functions in rheumatoid arthritis. J Autoimmun. 2018;87:69–81. Epub 2017/12/16. doi: 10.1016/j.jaut.2017.12.006 29254845.

74. Kim K-W, Kim H-R, Park J-Y, Park J-S, Oh H-J, Woo Y-J, et al. Interleukin-22 promotes osteoclastogenesis in rheumatoid arthritis through induction of RANKL in human synovial fibroblasts. Arthritis & Rheumatism. 2012;64(4):1015–23. doi: 10.1002/art.33446 22034096

75. Moura RA, Cascão R, Perpétuo I, Canhão H, Sousa E, Mourão AF, et al. Cytokine profile in serum and synovial fluid of patients with established rheumatoid arthritis. Annals of the Rheumatic Diseases. 2010;69(Suppl 2):A51–A. doi: 10.1136/ard.2010.129643g

76. Yoshida Y, Tanaka T. Interleukin 6 and rheumatoid arthritis. Biomed Res Int. 2014;2014:698313. Epub 2014/01/12. doi: 10.1155/2014/698313 24524085.

77. Srirangan S, Choy EH. The role of interleukin 6 in the pathophysiology of rheumatoid arthritis. Ther Adv Musculoskelet Dis. 2010;2(5):247–56. doi: 10.1177/1759720X10378372 22870451.

78. Rajaei E, Mowla K, Hayati Q, Ghorbani A, Dargahi-Malamir M, Hesam S, et al. Evaluating the relationship between serum level of interleukin-6 and rheumatoid arthritis severity and disease activity. Curr Rheumatol Rev. 2019. Epub 2019/02/06. 30727900.

79. Matsumoto T, Tsurumoto T, Shindo H. Interleukin-6 levels in synovial fluids of patients with rheumatoid arthritis correlated with the infiltration of inflammatory cells in synovial membrane. Rheumatol Int. 2006;26(12):1096–100. doi: 10.1007/s00296-006-0143-2 16738904.

80. Sun W, Dong L, Kaneyama K, Takegami T, Segami N. Bacterial diversity in synovial fluids of patients with TMD determined by cloning and sequencing analysis of the 16S ribosomal RNA gene. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008;105(5):566–71. Epub 2008/02/21. doi: 10.1016/j.tripleo.2007.08.015 18206402.

81. Siala M, Jaulhac B, Gdoura R, Sibilia J, Fourati H, Younes M, et al. Analysis of bacterial DNA in synovial tissue of Tunisian patients with reactive and undifferentiated arthritis by broad-range PCR, cloning and sequencing. Arthritis Res Ther. 2008;10(2):R40. Epub 2008/04/14. doi: 10.1186/ar2398 18412942.

82. Kell DB, Pretorius E. On the translocation of bacteria and their lipopolysaccharides between blood and peripheral locations in chronic, inflammatory diseases: the central roles of LPS and LPS-induced cell death. Integr Biol (Camb). 2015;7(11):1339–77. doi: 10.1039/c5ib00158g 26345428.

83. Bhattacharyya M, Ghosh T, Shankar S, Tomar N. The conserved phylogeny of blood microbiome. Mol Phylogenet Evol. 2017;109:404–8. Epub 2017/02/12. doi: 10.1016/j.ympev.2017.02.001 28216014.

84. Mangul S, M Olde Loohuis L, Ori A, Jospin G, Koslicki D, Yang HT, et al. Total RNA Sequencing reveals microbial communities in human blood and disease specific effects. bioRxiv. 2016.

85. Païssé S, Valle C, Servant F, Courtney M, Burcelin R, Amar J, et al. Comprehensive description of blood microbiome from healthy donors assessed by 16S targeted metagenomic sequencing. Transfusion. 2016;56(5):1138–47. doi: 10.1111/trf.13477 26865079.

86. Potgieter M, Bester J, Kell DB, Pretorius E. The dormant blood microbiome in chronic, inflammatory diseases. FEMS Microbiol Rev. 2015;39(4):567–91. doi: 10.1093/femsre/fuv013 25940667.

87. Amar J, Lange C, Payros G, Garret C, Chabo C, Lantieri O, et al. Blood microbiota dysbiosis is associated with the onset of cardiovascular events in a large general population: the D.E.S.I.R. study. PLoS One. 2013;8(1):e54461. doi: 10.1371/journal.pone.0054461 23372728.

88. Rajendhran J, Shankar M, Dinakaran V, Rathinavel A, Gunasekaran P. Contrasting circulating microbiome in cardiovascular disease patients and healthy individuals. Int J Cardiol. 2013;168(5):5118–20. Epub 2013/08/02. doi: 10.1016/j.ijcard.2013.07.232 23962776.

89. Dinakaran V, Rathinavel A, Pushpanathan M, Sivakumar R, Gunasekaran P, Rajendhran J. Elevated levels of circulating DNA in cardiovascular disease patients: metagenomic profiling of microbiome in the circulation. PLoS One. 2014;9(8):e105221. Epub 2014/08/18. doi: 10.1371/journal.pone.0105221 25133738.

90. Sze MA, Tsuruta M, Yang SW, Oh Y, Man SF, Hogg JC, et al. Changes in the bacterial microbiota in gut, blood, and lungs following acute LPS instillation into mice lungs. PLoS One. 2014;9(10):e111228. Epub 2014/10/21. doi: 10.1371/journal.pone.0111228 25333938.

91. Jeon SJ, Cunha F, Vieira-Neto A, Bicalho RC, Lima S, Bicalho ML, et al. Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome. 2017;5(1):109. Epub 2017/08/25. doi: 10.1186/s40168-017-0328-9 28841911.

92. Martel J, Wu CY, Huang PR, Cheng WY, Young JD. Pleomorphic bacteria-like structures in human blood represent non-living membrane vesicles and protein particles. Sci Rep. 2017;7(1):10650. Epub 2017/09/06. doi: 10.1038/s41598-017-10479-8 28878382.

93. Hammad DB, Tonge DP. Molecular Characterisation of the Synovial Fluid Microbiome. bioRxiv. 2018. doi: 10.1101/405613


Článek vyšel v časopise

PLOS One


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#