Intestinal microbiota status in patients with type 2 diabetes mellitus depending on the presence of chronic pyelonephritis at pre-dialysis stages of chronic kidney disease – an observational case-control study
- Authors: Sturov N.V.1, Popov S.V.1, Kobalava Z.D.1, Belikov I.I.1, Zhukov V.A.1, Lyapunova T.V.1, Meleshkevich T.A.1
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Affiliations:
- Peoples’ Friendship University of Russia named after Patrice Lumumba
- Issue: Vol 32, No 2 (2025)
- Pages: 116-123
- Section: Original articles
- URL: https://journals.eco-vector.com/2073-4034/article/view/680189
- DOI: https://doi.org/10.18565/pharmateca.2025.2.116-123
- ID: 680189
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Abstract
Background: Type 2 diabetes mellitus (DM2) is one of the main causes of chronic kidney disease (CKD) and end-stage renal failure. The medical community continues to debate the possible impact of intestinal microbiota (IM) imbalances on CKD progression. IM is a collection of microorganisms that play an important role in maintaining the health of the macroorganism and participate in various physiological processes. One of the urgent problems is the study of the composition of IM in patients with CKD and DM2. Most studies of IM were conducted in patients with CKD stages 4-5. This article presents the results of a study of the state of IM in diabetic patients with CKD at pre-dialysis stages in combination with chronic pyelonephritis (CP), obtained by gas chromatography-mass spectrometry (GCMS) using the microbial marker mass spectrometry (MMMS) method.
Objective. Evaluation of the composition of IM in the Moscow population of patients with DM2 in combination with CP at pre-dialysis stages of CKD by GCMS of fecal samples using the MMMS method.
Materials and methods: The IM analysis was conducted from 2021 to 2024 in 69 patients (23 patients with DM2 and CKD stages 3-4; 9 with CKD stages 3-4 with DM2 in combination with CP; 23 with DM2 and CKD stage 2; 14 with DM2 and without CKD) and 26 healthy volunteers. Results: It was found that in patients with DM2 without CKD, compared with healthy volunteers, there was a significant decrease in the number of Prevotella spp., Propionibacterium jensenii and Bacteroides fragilis, as well as a significant increase in Bacillus megaterium (Priestia megaterium) (p<0.05). In the group of patients with DM2 and stage 2 CKD, compared with patients with DM2 only, an increase in the number of Fusobacterium spp./Haemophilus spp. (p<0.05) was found. Comparison of patients with DM2 and stage 3–4 CKD with patients with DM2 and stage 2 CKD showed a decrease in Lactobacillus spp. and Ruminococcus spp. in the group of DM2 and stage 3–4 CKD. At the same time, these patients showed a significant increase in Propionibacterium acnes (Cutibacterium acnes) and Actinomyces spp. (p<0.05). In patients with DM2 and stage 3–4 CKD with exacerbation of chronic pyelonephritis who received antimicrobial therapy, a significant increase in the number of Rhodococcus spp., total microbial load, total bacterial load, anaerobes and Peptostreptococcus anaerobius 18623 was found compared to patients with DM2 and stage 3-4 CKD without CP (all p < 0.05).
Conclusion: In this study, for the first time in the Moscow population, the composition of IM in patients with DM2 at various pre-dialysis stages of CKD was studied and compared. The results obtained determine the need for further study of the role of IM and the prognostic value of its changes in the progression of CKD.
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About the authors
N. V. Sturov
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: sturov_nv@pfur.ru
ORCID iD: 0000-0002-3138-8410
Cand. Sci. (Med.), Associate Professor, Head of the Department of General Practice, Institute of Medicine
Russian Federation, MoscowSergey V. Popov
Peoples’ Friendship University of Russia named after Patrice Lumumba
Author for correspondence.
Email: popov_serv@pfur.ru
ORCID iD: 0000-0002-0567-4616
Dr. Sci. (Med.), Professor of the Department of General Practice, Institute of Medicine
Russian Federation, MoscowZh. D. Kobalava
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: kobalava_zhd@pfur.ru
ORCID iD: 0000-0002-5873-1768
Dr. Sci. (Med.), Professor, Corresponding Member of the Russian Academy of Sciences, Head of the Department of Internal Diseases with a course in Cardiology and Functional Diagnostics named after Academician V. S. Moiseev, Institute of Medicine, Head of the Institute of Clinical Medicine
Russian Federation, MoscowI. I. Belikov
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: belikov_ii@pfur.ru
ORCID iD: 0000-0001-5141-2193
Assistant of the Department of General Practice, Institute of Medicine
Russian Federation, MoscowV. A. Zhukov
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: zhukov_vlan@rudn.ru
ORCID iD: 0000-0001-9995-264X
Cand. Sci. (Med.), Associate Professor of the Department of General Practice, Institute of Medicine
Russian Federation, MoscowT. V. Lyapunova
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: lyapunova_tv@pfur.ru
ORCID iD: 0000-0002-1141-0764
Cand. Sci. (Med.), Associate Professor of the Department of Medical Informatics and Telemedicine, Institute of Medicine
Russian Federation, MoscowT. A. Meleshkevich
Peoples’ Friendship University of Russia named after Patrice Lumumba
Email: meleshkevich_ta@pfur.ru
ORCID iD: 0000-0003-3229-3357
Cand. Sci. (Med.), Associate Professor of the Department of Hospital Therapy with Courses in Endocrinology, Hematology and Clinical Laboratory Diagnostics, Medical Institute
Russian Federation, MoscowReferences
- Ассоциация нефрологов. Клинические рекомендации. Хроническая болезнь почек (ХБП). Москва: Министерство Здравоохранения Российской Федерации; 2024. [Association of Nephrologists. Clinical guidelines for Chronic kidney disease (CKD). Moscow: Ministry of Health of the Russian Federation; 2024. (In Russ.)]
- Krukowski H., Valkenburg S., Madella A.M., et al. Gut microbiome studies in CKD: opportunities, pitfalls and therapeutic potential. Nature Reviews Nephrology. 2023;19(2):87–101. doi: 10.1038/s41581-022-00647-z.
- Шутов Е.В, Большаков С.А, Макарова Т.А, и др. Микробиота кишечника и заболевания почек. Обзор литературы. Нефрология и диализ. 2024;26(3):283–302. [Shutov E.V, Bol’shakov S.A, Makarova T.A., et al. Intestinal microbiota and kidney diseases. Literature review. Nefrologiya i dializ. 2024;26(3):283–302. (In Russ.)]. doi: 10.28996/2618-9801-2024-3-283-302.
- Wong J., Piceno Y.M., DeSantis T.Z., et al. Expansion of urease- and uricase-containing, indole- and p-cresol-forming and contraction of short-chain fatty acid-producing intestinal microbiota in ESRD. Am J Nephrol. 2014;39(3):230–237. doi: 10.1159/000360010.
- Xu K.-Y., Xia G.-H., Lu J.-Q., et al. Impaired renal function and dysbiosis of gut microbiota contribute to increased trimethylamine-N-oxide in chronic kidney disease patients. Sci Rep. 2017;7(1):1445. doi: 10.1038/s41598-017-01387-y.
- Stadlbauer V., Horvath A., Ribitsch W., et al. Structural and functional differences in gut microbiome composition in patients undergoing haemodialysis or peritoneal dialysis. Sci Rep. 2017;7(1):15601. doi: 10.1038/s41598-017-15650-9.
- Vaziri N.D., Yuan J., Nazertehrani S., et al. Chronic kidney disease causes disruption of gastric and small intestinal epithelial tight junction. Am J Nephrol. 2013;38(2):99–103. doi: 10.1159/000353764.
- Vaziri N.D., Zhao Y.-Y., Pahl M.V. Altered intestinal microbial flora and impaired epithelial barrier structure and function in CKD: the nature, mechanisms, consequences and potential treatment. Nephrol Dial Transplant. 2016;31(5):737–746. doi: 10.1093/ndt/gfv095.
- Wang I.-K., Lai H.-C., Yu C.-J., et al. Real-Time PCR Analysis of the Intestinal Microbiotas in Peritoneal Dialysis Patients. Appl Environ Microbiol. 2012;78(4):1107–1112. doi: 10.1128/AEM.05605-11.
- Lun H., Yang W., Zhao S., et al. Altered gut microbiota and microbial biomarkers associated with chronic kidney disease. Microbiologyopen. 2019;8(4):1107-12. doi: 10.1002/mbo3.678.
- Tidjani Alou M., Naud S., Khelaifia S., et al. State of the Art in the Culture of the Human Microbiota: New Interests and Strategies. Clin Microbiol Rev. 2020;34(1).doi: 10.1128/cmr.00129-19.
- Хафизов К.Ф., Сперанская А.С, Мацвай А.Д, и др. Передовые технологии в диагностике вирусных заболеваний неясной этиологии. Инфекция и иммунитет. 2020;10(1):9–25. [Khafizov K.F., Speranskaya A.S, Matsvai A.D, et al. Advanced technologies in the diagnosis of viral diseases of unknown etiology. Infektsiya i immunitet. 2020;10(1):9–25. (In Russ.)]. doi: 10.15789/2220-7619-ATI-824.
- Бойко Н.Б., Гриневич В.Б., Федосова Н.Ф., и др. Методика масс-спектрометрии микробных маркеров как способ оценки пристеночной кишечной микробиоты при заболеваниях органов пищеварения. Учебно-методическое пособие. СПб., 2013. [Boiko N.B., Grinevich V.B., Fedosova N.F., et al. The technique of mass spectrometry of microbial markers as a way to assess the intestinal microbiota in diseases of the digestive system. Educational and methodological manual. St. Petersburg, 2013. (In Russ.)]
- Ситкин С.И., Вахитов Т.Я., Ткаченко Е.И. и др. Филометаболическое ядро микробиоты кишечника. Альманах клинической медицины. 2015;40:12?34. [Sitkin S.I., Vakhitov T.Ya., Tkachenko E.I. et al. Phylometabolic core of intestinal microbiota. Al’manakh klinicheskoi meditsiny. 2015;(40):12–34. (In Russ.)]. doi: 10.18786/2072-0505-2015-40-12-34.
- Демидова Т.Ю., Ардатская М.Д. Дисфункция филометаболического ядра микробиоты в патогенезе сахарного диабета 2 типа. FOCUS Эндокринология. 2021;3:16–23. [Demidova T.Yu., Ardatskaya M.D. The phylometabolic core of intestinal microbiota dysfunction in the pathogenesis of diabetes mellitus. FOCUS Endokrinologiya. 2021;3:16–23. (In Russ.)]. doi: 10.47407/ef2021.2.3.0030.
- Jeyaraman M., Mariappan T., Jeyaraman N., et al. Gut microbiome: а revolution in type II diabetes mellitus. World J Diabetes. 2024;15(9):1874–1888. doi: 10.4239/wjd.v15.i9.1874.
- Чижков П.А., Лагутина С.Н., Котова Ю. А., и др. Особенности разнообразия кишечной микробиоты у пациентов пожилого возраста с метаболическими нарушениями (обзор литературы). Научные результаты биомедицинских исследований. 2023;9(3):366–382. [Chizhkov P. A., Lagutina S. N., Kotova Yu.А. et al. Features of the diversity of the intestinal microbiota in elderly patients with metabolic disorders (literature review). Nauchnye rezul’taty biomeditsinskikh issledovanii. 2023;9(3):366?382. (In Russ.)]. doi: 10.18413/2658-6533-2023-9-3-0-7.
- Dyshlyuk L.S., Milentyeva I.S., Asyakina L.K., et al. Using bifidobacterium and propionibacterium strains in probiotic consortia to normalize the gastrointestinal tract. Braz J Biol. 2022;84:e256945. doi: 10.1590/1519-6984.256945.
- Zhao J., Ning X., Liu B., et al. Specific alterations in gut microbiota in patients with chronic kidney disease: an updated systematic review. Renal Failure. 2021;43(1):102–112. doi: 10.1080/0886022X.2020.1864404.
- Айтбаев К.А., Муркамилов И.Т., Фомин В.В. и др. Воспаление при хронической болезни почек: источники, последствия и противовоспалительная терапия. Клиническая медицина. 2018;4:314–320. [Aitbaev K. A., Murkamilov I. T., Fomin V. et al. Inflammation in chronic kidney disease: sources, consequences, and anti-inflammatory therapy. Klinicheskaya meditsina. 2018;4:314–320. (In Russ.)]. doi: 10.18821/0023-2149-2018-96-4-314-320.
- Стуров Н.В., Попов С.В., Беликов И.И. и др. Состояние кишечной микробиоты у пациентов с хронической болезнью почек. Современная наука: актуальные проблемы теории и практики. Серия: Естественные и технические науки. 2022;2-2:199–202. [Sturov N.V., Popov S.V., Belikov I.I., et al. The state of the intestinal microbiota in patients with chronic kidney disease. Sovremennaya nauka: aktual’nye problemy teorii i praktiki. Seriya: Estestvennye i tekhnicheskie nauki. 2022;2-2:199–202. (In Russ.)]. doi: 10.37882/2223-2966.2022.02.33.
- Лукичев Б.Г, Румянцев А.Ш, Панина И.Ю. и др. Микробиота кишечника и хроническая болезнь почек. Сообщение второе. Нефрология. 2019;23(1):18–31. [Lukichev B.G, Rumyantsev A.Sh, Panina I.Yu, et al. Intestinal microbiota and chronic kidney disease. The second message. Nefrologiya 2019;23(1):18–31. (In Russ.)]. doi: 10.24884/1561-6274-2019-23-1-18-31.
- Sturov N.V., Popov S.V., Belikov I.I. Gut microbiota and the ways to correct it in chronic kidney disease. Indian J Nephrol. 2023;33(3):162–169. doi: 10.4103/ijn.ijn_469_21.
- Покровская Е.В., Шамхалова М.Ш., Шестакова М.В. Новые взгляды на состояние кишечной микробиоты при ожирении и сахарном диабете 2 типа. Сахарный диабет. 2019;22(3):253–262. [Pokrovskaya E.V., Shamkhalova M.Sh, Shestakova M.V. New views on the state of the intestinal microbiota in obesity and type 2 diabetes mellitus. Sakharnyi diabet. 2019;22(3):253–262. (In Russ.)] doi: 10.14341/DM10194.
- Sadagopan A., Mahmoud A., Begg M., et al. Understanding the role of the gut microbiome in diabetes and therapeutics targeting leaky gut: a systematic review. 2023;15(7):e41559. doi: 10.7759/cureus.41559.
- Yu J.-X., Chen X., Zang S.-G., et al. Gut microbiota microbial metabolites in diabetic nephropathy patients: far to go. Front Cell Infect Microbiol. 2024;14:1359432. doi: 10.3389/fcimb.2024.1359432.
- Демидова Т.Ю., Лобанова К.Г., Ойноткинова О.Ш. Кишечная микробиота как фактор риска развития ожирения и сахарного диабета 2 типа. Терапевтический архив. 2020;10:97–104. [Demidova T. Y., Lobanova K.G., Oinotkinova O.S. Intestinal microbiota as a risk factor for developing obesity and type 2 diabetes. Terapevticheskii arkhiv. 2020;10:97–104. (In Russ.)]. doi: 10.26442/00403660.2020.10.000778.
- Bhargava S., Merckelbach E., Noels H., et al. Homeostasis in the Gut Microbiota in Chronic Kidney Disease. Toxins. 2022;14(10):648. doi: 10.3390/toxins14100648.
- Voroneanu L., Burlacu A., Brinza C., et al. Gut microbiota in chronic kidney disease: from composition to modulation towards better outcomes - а systematic review. J Clin Med. 2023;12(5):1948. doi: 10.3390/jcm12051948.
- Alhhazmi A.A., Alhamawi R.M., Almisned R.M., et al. Gut microbial and associated metabolite markers for colorectal cancer diagnosis. Microorganisms. 2023;11(8):2037. doi: 10.3390/microorganisms11082037.
- Методические рекомендации MP 2.3.1.0253-21 Нормы физиологических потребностей в энергии и пищевых веществах для различных групп населения Российской Федерации (утв. Федеральной службой по надзору в сфере защиты прав потребителей и благополучия человека 22 июля 2021 г.). [Methodological recommendations MP 2.3.1.0253-21 Norms of physiological energy and nutritional requirements for Various Groups of the population of the Russian Federation (approved by the Federal Service for Supervision of Consumer Rights Protection and Human Welfare on July 22, 2021) (In Russ.)].
- Халиуллина С.В., Анохин В.А., Поздеев О.К. и др. Кишечный дисбиоз – этиологическая и патогенетическая основа синдрома бактериурии. Казанский медицинский журнал. 2003;1:51–53. [Khaliullina S. V., Anokhin V. A., Pozdeev O. K. Intestinal dysbiosis-the etiological and pathogenetic basis of bacteriuria syndrome. Kazanskiy meditsinskiy zhurnal=Kazan Medical Journal. 2003;1:51–53. (In Russ.)]
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