THE ROLE OF MICROBIOME IN RHEUMATOID ARTHRITIS DEVELOPMENT. A REVIEW.
Relevance. Rheumatoid arthritis (RA) is a chronic, autoimmune disease characterized by symmetrical deforming arthritis and systemic manifestations, such as damage to the cardiovascular, respiratory systems, and skin. The prevalence of RA is high. Worldwide incidence ranges from 0.24 to 1% of the population. The disease is 2–3 times more common in women than in men. The peak incidence occurs in working age, from 35 to 64 years. Untreated RA can lead not only to patient disability, but also to death. In this connection, RA is a pressing problem of modern medicine. In recent years, the influence of epigenetic factors on the development of RA, including the influence of the microbiome, has been actively studied.
Purpose: The role of the oral and intestinal microbiome in the development of rheumatoid arthritis.
Search strategy: A search for scientific publications was carried out in the following databases of scientific publications and specialized search engines: PubMed, Google Scholar, Web of Science, Cochrane Library. A number of original publicly available publications on the research topic were analyzed. The search depth was 15 years. As a result of the search, we studied 459 foreign publications, of which 97 publications were included in this review. Inclusion criteria: meta-analyses, systematic reviews, cohort and cross-sectional studies. Exclusion criteria: short reports, newspaper articles and expert opinion in the form of short reports.
Results and conclusions: Based on the results of the review, it was revealed that in RA there is a change in the composition of the microbiome of both the oral cavity and the intestines. Experimental studies have revealed the role of the microbiome in the pathogenesis of RA development. In particular, the role of oral cavity-dwelling Porphyromonas gingivalis (P.gingivalis), Aggregatibacter actinomycetemcomitans (Aa), as well as gut microbiome representatives Prevotella copri (P. copri), Collinsella aerofaciens, Proteobacteria, Clostridium cluster XlVa and Ruminococcus genus.
Aigerim К. Ibrayeva1, https://orcid.org/0000-0003-0628-9370
Natalya A. Latypova1, https://orcid.org/0000-0003-4283-4911
Almagul R. Kushugulova2, https://orcid.org/0000-0001-9479-0899
Assel M. Meiramova1, https://orcid.org/0000-0002-4030-0783
Argul A. Isilbayeva2, https://orcid.org/0000-0002-7350-6083
Samat S. Kozhahmetov2, https://orcid.org/0000-0001-9668-0327
1 NCJSC "Astana Medical University", Astana, Republic of Kazakhstan;
2 AEO «Nazarbayev University», Astana, Republic of Kazakhstan.
1. Aas J.A., Paster B.J., Stokes L.N., Olsen I., Dewhirst F.E. Defining the Normal Bacterial Flora of the Oral Cavity // J Clin Microbiol. 2005. 43(11):5721-5732.
2. AIHW; Australian Institute of Health Welfare. Rheumatoid Arthritis. Available online: https://www.aihw.gov.au/reports/ chronic-musculoskeletal-conditions/rheumatoid-arthritis (accessed on 10 April 2021).
3. Ajeganova S., Huizinga T. Sustained remission in rheumatoid arthritis: latest evidence and clinical considerations // Ther Adv Musculoskelet Dis. 2017. 9(10):249-262.
4. Alghamdi M.A., Redwan E.M. Interplay of Microbiota and Citrullination in the Immunopathogenesis of Rheumatoid Arthritis // Probiotics Antimicrob Proteins. 2022. 14(1):99-113.
5. Araújo V.M.A., Melo I.M., Lima V. Relationship between Periodontitis and Rheumatoid Arthritis: Review of the Literature // Mediators Inflamm. 2015. 2015:1-15.
6. Äyräväinen L., Leirisalo-Repo M., Kuuliala A. et al. Periodontitis in early and chronic rheumatoid arthritis: a prospective follow-up study in Finnish population // BMJ Open. 2017. 7(1):e011916.
7. Beam A., Clinger E., Hao L. Effect of Diet and Dietary Components on the Composition of the Gut Microbiota // Nutrients. 2021. 13(8):2795.
8. Bello-Gualtero J.M., Lafaurie G.I., Hoyos L.X. et al. Periodontal Disease in Individuals With a Genetic Risk of Developing Arthritis and Early Rheumatoid Arthritis: A Cross-Sectional Study // J Periodontol. 2016. 87(4):346-356.
9. Cai Y., Zhang J., Liang J. et al. The Burden of Rheumatoid Arthritis: Findings from the 2019 Global Burden of Diseases Study and Forecasts for 2030 by Bayesian Age-Period-Cohort Analysis // J Clin Med. 2023. 12(4):1291.
10. Campbell C., Kandalgaonkar M.R., Golonka R.M., Yeoh B.S., Vijay-Kumar M., Saha P. Crosstalk between Gut Microbiota and Host Immunity: Impact on Inflammation and Immunotherapy // Biomedicines. 2023. 11(2):294.
11. Catrina A.I., Joshua V., Klareskog L., Malmström V. Mechanisms involved in triggering rheumatoid arthritis // Immunol Rev. 2016. 269(1):162-174.
12. Chen J., Wright K., Davis J.M. et al. An expansion of rare lineage intestinal microbes characterizes rheumatoid arthritis // Genome Med. 2016. 8(1):43.
13. Chen Y., Ma C., Liu L. et al. Analysis of gut microbiota and metabolites in patients with rheumatoid arthritis and identification of potential biomarkers // Aging. 2021.13(20):23689-23701.
14. Cheng Z., Meade J., Mankia K., Emery P., Devine D.A. Periodontal disease and periodontal bacteria as triggers for rheumatoid arthritis // Best Pract Res Clin Rheumatol. 2017. 31(1):19-30.
15. Clarke J. Disease onset goes with its gut in RA // Nat Rev Rheumatol. 2020. 16(7):350-350.
16. Courbon G., Rinaudo-Gaujous M., Blasco-Baque V., et al. Porphyromonas gingivalis experimentally induces periodontis and an anti-CCP2-associated arthritis in the rat // Ann Rheum Dis. 2019. 78(5):594-599.
17. Cristofori F., Dargenio V.N., Dargenio C., Miniello V.L., Barone M., Francavilla R. Anti-Inflammatory and Immunomodulatory Effects of Probiotics in Gut Inflammation: A Door to the Body // Front Immunol. 2021. 12:578386.
18. Cross M., Smith E., Hoy D. et al. The global burden of rheumatoid arthritis: estimates from the Global Burden of Disease 2010 study. // Annals of the Rheumatic Diseases, 73(7), 1316–1322. doi:10.1136/annrheumdis-2013-204627
19. Dewhirst F.E., Chen T., Izard J. et al. The Human Oral Microbiome // J Bacteriol. 2010. 192(19):5002-5017.
20. Du Q., Liu X.H., Tian K., Meng S. [Analysis of Periodontal Status and Salivary Microbial Diversity in Patients with Rheumatoid Arthritis] // Sichuan Da Xue Xue Bao Yi Xue Ban. 2019. 50(6):935-940.
21. Eckburg P.B., Bik E.M., Bernstein C.N., et al. Diversity of the Human Intestinal Microbial Flora // Science. 2005. 308(5728):1635-1638.
22. Engström M., Eriksson K., Lee L. et al. Increased citrullination and expression of peptidylarginine deiminases independently of P. gingivalis and A. actinomycetemcomitans in gingival tissue of patients with periodontitis // J Transl Med. 2018. 16(1):214.
23. Evans‐Marin H., Rogier R., Koralov S.B. et al. Microbiota‐Dependent Involvement of Th17 Cells in Murine Models of Inflammatory Arthritis // Arthritis Rheumatol. 2018. 70(12):1971-1983.
24. Fuggle N.R., Smith T.O., Kaul A., Sofat N. Hand to Mouth: A Systematic Review and Meta-Analysis of the Association between Rheumatoid Arthritis and Periodontitis // Front Immunol. 2016. 7. р. 80-97.
25. Gallo P.M., Rapsinski G.J., Wilson R.P. et al. Amyloid-DNA Composites of Bacterial Biofilms Stimulate Autoimmunity // Immunity. 2015. 42(6):1171-1184.
26. Gautam A., Kumar R., Chakraborty N. et al. Altered fecal microbiota composition in all male aggressor‐exposed rodent model simulating features of post‐traumatic stress disorder // J Neurosci Res. 2018. 96(7):1311-1323.
27. González‐Febles J., Sanz M. Periodontitis and rheumatoid arthritis: What have we learned about their connection and their treatment? // Periodontol. 2000. 2021. 87(1):181-203.
28. Gul H.L., Eugenio G., Rabin T. et al. Defining remission in rheumatoid arthritis: does it matter to the patient? A comparison of multi-dimensional remission criteria and patient reported outcomes // Rheumatology. Published online August 19, 2019:kez330.
29. Hashimoto M., Yamazaki T., Hamaguchi M. et al. Periodontitis and Porphyromonas gingivalis in Preclinical Stage of Arthritis Patients. Heymann D, ed. // PLOS ONE. 2015. 10(4):e0122121.
30. Holt S.C., Ebersole J., Felton J., Brunsvold M., Kornman K.S. Implantation of Bacteroides gingivalis in Nonhuman Primates Initiates Progression of Periodontitis // Science. 1988. 239(4835):55-57.
31. Horta-Baas G., Romero-Figueroa M.D.S., Montiel-Jarquín A.J., Pizano-Zárate M.L., García-Mena J., Ramírez-Durán N. Intestinal Dysbiosis and Rheumatoid Arthritis: A Link between Gut Microbiota and the Pathogenesis of Rheumatoid Arthritis // J Immunol Res. 2017. 2017:1-13.
32. Hua R., Ni Q., Eliason T.D. et al. Biglycan and chondroitin sulfate play pivotal roles in bone toughness via retaining bound water in bone mineral matrix // Matrix Biol. 2020. 94:95-109.
33. Ito Y., Hashimoto M., Hirota K. et al. Detection of T cell responses to a ubiquitous cellular protein in autoimmune disease // Science. 2014. 346(6207):363-368.
34. Jang S., Kwon E.J., Lee J.J. Rheumatoid Arthritis: Pathogenic Roles of Diverse Immune Cells // Int J Mol Sci. 2022. 23(2):905.
35. Jasemi S., Erre G.L., Cadoni M.L., Bo M., Sechi L.A. Humoral Response to Microbial Biomarkers in Rheumatoid Arthritis Patients // J Clin Med. 2021. 10(21):5153.
36. Johansson A. Aggregatibacter actinomycetemcomitans Leukotoxin: A Powerful Tool with Capacity to Cause Imbalance in the Host Inflammatory Response // Toxins. 2011. 3(3):242-259.
37. Johansson L., Sherina N., Kharlamova N. et al. Concentration of antibodies against Porphyromonas gingivalis is increased before the onset of symptoms of rheumatoid arthritis // Arthritis Res Ther. 2016. 18(1):201.
38. Kamada N., Seo S.U., Chen G.Y., Núñez G. Role of the gut microbiota in immunity and inflammatory disease // Nat Rev Immunol. 2013. 13(5):321-335.
39. Kim H., McCulloch C.A. Filamin A mediates interactions between cytoskeletal proteins that control cell adhesion // FEBS Lett. 2011. 585(1):18-22.
40. Konig M.F., Abusleme L., Reinholdt J. et al. Aggregatibacter actinomycetemcomitans – induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis // Sci Transl Med. 2016. 8(369).
41. Kulkarni A., Beckler M.D., Amini S.S., Kesselman MM. Oral Microbiome in Pre-Rheumatoid Arthritis: The Role of Aggregatibacter Actinomycetemcomitans in Bacterial Composition // Cureus. Published online December 5, 2022.
42. Laugisch O., Wong A., Sroka A. et al. Citrullination in the periodontium—a possible link between periodontitis and rheumatoid arthritis // Clin Oral Investig. 2016. 20(4):675-683.
43. Li Y., Guo R., Oduro P.K. et al. The Relationship Between Porphyromonas Gingivalis and Rheumatoid Arthritis: A Meta-Analysis // Front Cell Infect Microbiol. 2022. 12:956417.
44. Li Y., Zhang S.X., Yin X.F. et al. The Gut Microbiota and Its Relevance to Peripheral Lymphocyte Subpopulations and Cytokines in Patients with Rheumatoid Arthritis. Xu B, ed. // J Immunol Res. 2021. 2021:1-9.
45. Liu X., Zeng B., Zhang J. et al. Role of the Gut Microbiome in Modulating Arthritis Progression in Mice // Sci Rep. 2016. 6(1):30594.
46. Liu X., Zou Q., Zeng B. Analysis of Fecal Lactobacillus Community Structure in Patients with Early Rheumatoid Arthritis // Curr Microbiol. 2013. 67(2):170-176.
47. Looh S.C., Soo Z.M.P., Wong J.J., Yam H.C., Chow S.K., Hwang J.S. Aggregatibacter actinomycetemcomitans as the Aetiological Cause of Rheumatoid Arthritis: What Are the Unsolved Puzzles? // Toxins. 2022. 14(1):50.
48. Lopez-Oliva I., Paropkari A.D., Saraswat S. et al. Dysbiotic Subgingival Microbial Communities in Periodontally Healthy Patients With Rheumatoid Arthritis. Arthritis Rheumatol. 2018. 70(7):1008-1013.
49. Lourbakos A., Chinni C., Thompson P. et al. Cleavage and activation of proteinase-activated receptor-2 on human neutrophils by gingipain-R from Porphyromonas gingivalis // FEBS Lett. 1998. 435(1):45-48.
50. Maeda Y., Kurakawa T., Umemoto E. et al. Dysbiosis Contributes to Arthritis Development via Activation of Autoreactive T Cells in the Intestine: Dysbiosis contributes to arthritis development // Arthritis Rheumatol. 2016. 68(11):2646-2661.
51. Maekawa T., Krauss J.L., Abe T. et al. Porphyromonas gingivalis Manipulates Complement and TLR Signaling to Uncouple Bacterial Clearance from Inflammation and Promote Dysbiosis // Cell Host Microbe. 2014. 15(6):768-778.
52. Marchesan J.T., Gerow E.A., Schaff R. et al. Porphyromonas gingivalis oral infection exacerbates the development and severity of collagen-induced arthritis // Arthritis Res Ther. 2013. 15(6):R186.
53. Martínez-Rivera J.I., Xibillé-Friedmann D.X. et al. Salivary ammonia levels and Tannerella forsythia are associated with rheumatoid arthritis: A cross sectional study // Clin Exp Dent Res. 2017. 3(3):107-114.
54. McGraw W.T., Potempa J., Farley D., Travis J. Purification, Characterization, and Sequence Analysis of a Potential Virulence Factor from Porphyromonas gingivalis , Peptidylarginine Deiminase. Burns DL, ed. // Infect Immun. 1999. 67(7):3248-3256.
55. Mena-Vázquez N., Ruiz-Limón P. et al., Fernández-Nebro A. Expansion of Rare and Harmful Lineages is Associated with Established Rheumatoid Arthritis // J Clin Med. 2020. 9(4):1044.
56. Mikuls T.R., Payne J.B., Yu F. et al. Periodontitis and Porphyromonas gingivalis in Patients With Rheumatoid Arthritis: Periodontitis and P gingivalis in RA // Arthritis Rheumatol. 2014. 66(5):1090-1100.
57. Nelson J., Sjöblom H., Gjertsson I., Ulven S.M., Lindqvist H.M., Bärebring L. Do Interventions with Diet or Dietary Supplements Reduce the Disease Activity Score in Rheumatoid Arthritis? A Systematic Review of Randomized Controlled Trials // Nutrients. 2020. 12(10):2991.
58. Nielen M.M.J. Simultaneous development of acute phase response and autoantibodies in preclinical rheumatoid arthritis // Ann Rheum Dis. 2006. 65(4):535-537.
59. Otón T., Carmona L. The epidemiology of established rheumatoid arthritis // Best Pract Res Clin Rheumatol. 2019. 33(5):101477.
60. Paster B.J., Boches S.K., Galvin J.L. et al. Bacterial Diversity in Human Subgingival Plaque // J Bacteriol. 2001. 183(12):3770-3783.
61. Pianta A., Arvikar S., Strle K. et al. Evidence of the Immune Relevance of Prevotella copri , a Gut Microbe, in Patients With Rheumatoid Arthritis // Arthritis Rheumatol. 2017. 69(5):964-975.
62. Pianta A., Arvikar S.L., Strle K. et al. Two rheumatoid arthritis–specific autoantigens correlate microbial immunity with autoimmune responses in joints // J Clin Invest. 2017. 127(8):2946-2956.
63. Picchianti-Diamanti A., Panebianco C., Salemi S. et al. Analysis of Gut Microbiota in Rheumatoid Arthritis Patients: Disease-Related Dysbiosis and Modifications Induced by Etanercept // Int J Mol Sci. 2018. 19(10):2938.
64. Rapsinski G.J., Wynosky-Dolfi M.A., Oppong G.O. et al. Toll-Like Receptor 2 and NLRP3 Cooperate To Recognize a Functional Bacterial Amyloid, Curli. Bäumler AJ, ed. // Infect Immun. 2015. 83(2):693-701.
65. Reichert S., Haffner M., Keyßer G. et al. Detection of oral bacterial DNA in synovial fluid // J Clin Periodontol. 2013. 40(6):591-598.
66. Reichert S., Jurianz E., Natalie P. et al. Is periodontitis a prognostic factor in order to indicate antibodies against citrullinated peptides in patients with rheumatoid arthritis? // Clin Exp Rheumatol. 2020. 38(2):227-238.
67. Reparon-Schuijt C.C. et al. Secretion of anti-citrulline-containing peptide antibody by B lymphocytes in rheumatoid arthritis. Arthritis Rheum. 2001. 44(1):41-47.
68. Safiri S., Kolahi A.A., Hoy D. et al. Global, regional and national burden of rheumatoid arthritis 1990–2017: a systematic analysis of the Global Burden of Disease study 2017 // Ann Rheum Dis. 2019. 78(11):1463-1471.
69. Scher J.U., Sczesnak A., Longman R.S. et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife. 2013. 2:e01202.
70. Scher J.U., Ubeda C., Equinda M. et al. Periodontal disease and the oral microbiota in new-onset rheumatoid arthritis // Arthritis Rheum. 2012. 64(10):3083-3094.
71. Scherer H.U., Häupl T., Burmester G.R. The etiology of rheumatoid arthritis // J Autoimmun. 2020. 110:102400.
72. Schlafer S., Meyer R.L., Dige I., Regina V.R. Extracellular DNA Contributes to Dental Biofilm Stability // Caries Res. 2017. 51(4):436-442.
73. Shanahan F., Ghosh T.S., O’Toole P.W. The Healthy Microbiome - What Is the Definition of a Healthy Gut Microbiome? // Gastroenterology. 2021. 160(2):483-494.
74. Singh R.K., Chang H.W., Yan D. et al. Influence of diet on the gut microbiome and implications for human health // J Transl Med. 2017. 15(1):73.
75. Smolen J.S., Aletaha D., Barton A. et al. Rheumatoid arthritis // Nat Rev Dis Primer. 2018. 4(1):18001.
76. Socransky S.S., Haffajee A.D., Cugini M.A., Smith C., Kent R.L. Microbial complexes in subgingival plaque // J Clin Periodontol. 1998. 25(2):134-144.
77. Song X., Sun X., Oh S.F. et al. Microbial bile acid metabolites modulate gut RORγ+ regulatory T cell homeostasis // Nature. 2020. 577(7790):410-415.
78. Taglialegna A., Lasa I., Valle J. Amyloid Structures as Biofilm Matrix Scaffolds. O’Toole GA, ed. // J Bacteriol. 2016. 198(19):2579-2588.
79. Tajik N., Frech M., Schulz O. et al. Targeting zonulin and intestinal epithelial barrier function to prevent onset of arthritis // Nat Commun. 2020. 11(1):1995.
80. Tan T.G., Sefik E. et al. Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice // Proc Natl Acad Sci. 2016. 113(50).
81. Tar I., Csősz É., Végh E. et al. Salivary citrullinated proteins in rheumatoid arthritis and associated periodontal disease. Sci Rep. 2021. 11(1):13525.
82. Tong Y., Zheng L., Qing P. et al. Oral Microbiota Perturbations Are Linked to High Risk for Rheumatoid Arthritis // Front Cell Infect Microbiol. 2020. 9:475.
83. Totaro M., Cattani P., Ria F. et al. Porphyromonas gingivalis and the pathogenesis of rheumatoid arthritis: analysis of various compartments including the synovial tissue // Arthritis Res Ther. 2013. 15(3):R66.
84. Trombone A.P., Claudino M., Colavite P. et al. Periodontitis and arthritis interaction in mice involves a shared hyper-inflammatory genotype and functional immunological interferences // Genes Immun. 2010. 11(6):479-489.
85. Van De Sande M., De Hair M. et al. Different stages of rheumatoid arthritis: features of the synovium in the preclinical phase // Ann Rheum Dis. 2011. 70(5):772-777.
86. Volkov M., Dekkers J. et al. Comment on “Aggregatibacter actinomycetemcomitans – induced hypercitrullination links periodontal infection to autoimmunity in rheumatoid arthritis” // Sci Transl Med. 2018. 10(433):8349.
87. Wang P., Tao J.H., Pan H.F. Probiotic bacteria: a viable adjuvant therapy for relieving symptoms of rheumatoid arthritis // Inflammopharmacology. 2016. 24(5):189-196.
88. Wang Q., Zhang S.X., Chang M.J. et al. Characteristics of the Gut Microbiome and Its Relationship With Peripheral CD4+ T Cell Subpopulations and Cytokines in Rheumatoid Arthritis // Front Microbiol. 2022. 13:799602.
89. Wegner N., Wait R., Sroka A. et al. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and α-enolase: Implications for autoimmunity in rheumatoid arthritis // Arthritis Rheum. 2010. 62(9):2662-2672.
90. van der Woude D., van der Helm-van Mil A.H. Update on the epidemiology, risk factors, and disease outcomes of rheumatoid arthritis // Best Pract Res Clin Rheumatol. 2018. 32(2):174-187.
91. Wu D., Liu X., Su H., et al. Oral antigens induce rheumatoid arthritis-like inflammation in a rat model // Inflamm Res. 2013. 62(3):291-297.
92. Wu H.J., Ivanov I.I., Darce J. et al. Gut-Residing Segmented Filamentous Bacteria Drive Autoimmune Arthritis via T Helper 17 Cells // Immunity. 2010. 32(6):815-827.
93. Wu X., He B., Liu J. et al. Molecular Insight into Gut Microbiota and Rheumatoid Arthritis // Int J Mol Sci. 2016. 17(3):431.
94. Zhang X., Zhang D., Jia H. et al. The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment // Nat Med. 2015. 1(8):895-905.
95. Zhernakova A., Kurilshikov A., Bonder M.J. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity // Science. 2016. 352(6285):565-569.
96. Zhou L., Zhang M., Wang Y. et al. Faecalibacterium prausnitzii Produces Butyrate to Maintain Th17/Treg Balance and to Ameliorate Colorectal Colitis by Inhibiting Histone Deacetylase // Inflamm Bowel Dis. 2018. 24(9):1926-1940.
97. Zwicky P., Unger S., Becher B. Targeting interleukin-17 in chronic inflammatory disease: A clinical perspective // J Exp Med. 2020. 217(1):e20191123.
Количество просмотров: 580
Категория статей:
Обзор литературы
Библиографическая ссылка
Ibrayeva A.К., Latypova N.A., Kushugulova A.R., Meiramova A.M., Isilbayeva A.A., Kozhahmetov S.S. The role of microbiome in Rheumatoid arthritis development. A review // Nauka i Zdravookhranenie [Science & Healthcare]. 2023, (Vol.25) 6, pp. 191-198. DOI 10.34689/SH.2023.25.6.022Похожие публикации:
UNDERSTANDING OF RECURRENT RESPIRATORY INFECTIONS IN CHILDREN AT THE PRESENT STAGE. REVIEW.
ГЕМОДИНАМИЧЕСКИ ЗНАЧИМЫЙ ОТКРЫТЫЙ АРТЕРИАЛЬНЫЙ ПРОТОК У НЕДОНОШЕННЫХ НОВОРОЖДЕННЫХ ДЕТЕЙ. ОБЗОР ЛИТЕРАТУРЫ
RADIOIODINE-RESISTANT DIFFERENTIATED THYROID CANCER: CLINICOPATHOLOGICAL CHARACTERISTICS, MOLECULAR GENETIC ALTERATIONS. REVIEW.
ПРЕРЫВИСТАЯ КАТЕТЕРИЗАЦИЯ МОЧЕВОГО ПУЗЫРЯ КАК «ЗОЛОТОЙ СТАНДАРТ» ЛЕЧЕНИЯ НЕЙРОГЕННОГО МОЧЕВОГО ПУЗЫРЯ У ЛИЦ, С ПОВРЕЖДЕНИЕМ СПИННОГО МОЗГА
АНАЛИЗ ОПЫТА МЕДСЕСТЕР И ФАКТОРОВ, ВЛИЯЮЩИХ НА ДОБРОВОЛЬНОЕ СООБЩЕНИЕ ОБ ИНЦИДЕНТАХ