2713-2900 Вестник УГМУ USMU Medical Bulletin Уральский государственный медицинский университет 10.52420/usmumb.11.2.e00216 SVTGSI https://vestnikusmu.ru/index.php/vestnik/article/view/216 Видовой состав бифидобактерий толстой кишки у детей дошкольного возраста с психическим дизонтогенезом Species Composition of Bifidobacteria in the Colon of Preschool Children with Mental Dysontogenesis Лихачев Иван Алексеевич Лихачев Иван Алексеевич Likhachev Ivan A. ialihachev@yandex.ru 0009-0003-3034-4402 Ворошилина Екатерина Сергеевна Ворошилина Екатерина Сергеевна Voroshilina Ekaterina S. voroshilina@gmail.com 0000-0003-1630-1628 Зорников Данила Леонидович Зорников Данила Леонидович Zornikov Danila L. zornikovdl@yandex.ru 0000-0001-9132-215X Аминева Полина Геннадьевна Аминева Полина Геннадьевна Amineva Polina G. pga@qualitymed.ru 0000-0001-9752-5054 Сиденкова Алена Петровна Сиденкова Алена Петровна Sidenkova Alena P. sidenkovs@mail.ru 0000-0001-5142-3992 Саламатова Савелина Андреевна Саламатова Савелина Андреевна Salamatova Savelina A. savelina2000@yandex.ru 0009-0006-4603-2595 Уральский государственный медицинский университет (Екатеринбург, Россия) Ural State Medical University (Ekaterinburg, Russia) Уральский государственный медицинский университет; Медико-фармацевтический центр «Гармония» (Екатеринбург, Россия) Ural State Medical University; Medical and Pharmaceutical Center "Garmoniya" (Ekaterinburg, Russia) Уральский государственный медицинский университет; Кволити Мед (Екатеринбург, Россия) Ural State Medical University; Quality Med (Ekaterinburg, Russia) 30 06 2026 2026 11 2 e00216 21 05 2026 10 06 2026 25 05 2026 © Лихачев И.А., Ворошилина Е.С., Зорников Д.Л., Аминева П.Г., Сиденкова А.П., Саламатова С.А., 2026. Материал доступен по условиям лицензии CC BY-NC-SA 4.0 Int. 2026 Лихачев И.А., Ворошилина Е.С., Зорников Д.Л., Аминева П.Г., Сиденкова А.П., Саламатова С.А. Likhachev I.A., Voroshilina E.S., Zornikov D.L., Amineva P.G., Sidenkova A.P., Salamatova S.A. CC BY-NC-SA 4.0 https://vestnikusmu.ru/index.php/vestnik/article/view/216

Введение. Бифидобактерии — ключевая группа микроорганизмов толстой кишки у детей. Снижение их представленности в составе микробиоты толстой кишки ассоциировано с рядом соматических заболеваний, а также с психическим дизонтогенезом. Цель работы — оценить частоту выявления, количество и видовой состав Bifidobacterium spp. в микробиоте толстой кишки у детей дошкольного возраста с психическим дизонтогенезом. Материалы и методы. В исследование включены 157 здоровых детей и 81 ребенок с ПДО в возрасте от 4 до 7,8 лет (Ме = 5,8). Выявление и количественную оценку бифидобактерий проводили методом ПЦР в реальном времени (ПЦР-РВ) с помощью теста «Энтерофлор Дети». Статистическую обработку и визуализацию данных проводили с помощью R версии 4.6.0. Результаты. У детей с ПДО реже встречался B. bifidum (30,6 % против 45,7 %, p < 0,050), а также были снижены доли «взрослых» бифидобактерий (p = 0,043) и B. catenulatum (p = 0,017). Абсолютные количества этих таксонов не различались между группами. Заключение. У детей с ПДО снижены частота обнаружения B. bifidum и относительная доля B. catenulatum, тогда как на уровне рода Bifidobacterium различий нет. Изменения носят качественный характер.

Introduction. Bifidobacteria are a key group of microorganisms in the colon of children. A decrease in their abundance in the colonic microbiota is associated with a number of somatic diseases, as well as mental dysontogenesis. The purpose of the study is to evaluate the frequency of detection, quantity and species composition of Bifidobacterium spp. in the colon microbiota of preschool children with mental dysontogenesis. Materials and methods. The study included 157 healthy children and 81 children with MD, aged 4 to 7.8 years (Me = 5.8). Bifidobacteria were detected and quantified using real-time PCR (RT-PCR) using the Enteroflor Kiddy test. Statistical processing and data visualization were performed using R version 4.6.0. Results. In children with MD, B. bifidum was less common (30.6 % vs. 45.7 %, p < 0.050), and the proportions of “adult” bifidobacteria (p = 0.043) and B. catenulatum (p = 0.017) were also reduced. The absolute quantities of these taxa did not differ between the groups. Conclusion. In children with MD, the detection rate of B. bifidum and the relative proportion of B. catenulatum were reduced, whereas there were no differences at the level of the genus Bifidobacterium. The changes are qualitative in nature.

 Ключевые слова бифидобактерии психический дизонтогенез полимеразная цепная реакция Энтерофлор Дети Keywords bifidobacteria mental dysontogenesis polymerase chain reaction Enteroflor Kiddy Авторы выражают благодарность генеральному директору Медико-фармацевтического центра «Гармония» Л. В. Хаютину за возможность проведения лабораторных исследований на базе лабораторного отделения центра. Авторы заявляют об отсутствии внешнего финансирования. The authors express their gratitude to Leonid V. Khayutin, General Director of Medical and Pharmaceutical Center “Garmoniya”, for the opportunity to conduct laboratory research at the center’s laboratory department. The authors declare the absence of external funding for the study. Tatsiopoulou P, Serdari A, Bonti E, Zilikis N. Mental disorders in childhood and adolescence: A systematic review and meta-analysis of epidemiological data. BMC Psychiatry. 2025;25(1):1087. DOI: https://doi.org/10.1186/s12888-025-07532-6. Sacco R, Camilleri N, Eberhardt J, Umla-Runge K, Newbury-Birch D. A systematic review and meta-analysis on the prevalence of mental disorders among children and adolescents in Europe. European Child & Adolescent Psychiatry. 2024;33(9):2877–2894. DOI: https://doi.org/10.1007/s00787-022-02131-2. Njardvik U, Wergeland GJ, Riise EN, Hannesdottir DK, Öst LG. Psychiatric comorbidity in children and adolescents with ADHD: A systematic review and meta-analysis. Clinical Psychology Review. 2025;118:102571. DOI: https://doi.org/10.1016/j.cpr.2025.102571. Cryan JF, O’Riordan KJ, Cowan CS, Sandhu KV, Bastiaanssen TF, Boehme M, et al. The microbiota-gut-brain axis. Physiological Reviews. DOI: https://doi.org/10.1152/physrev.00018.2018. Jabbari Shiadeh SM, Chan WK, Rasmusson S, Hassan N, Joca S, Westberg L, et al. Bidirectional crosstalk between the gut microbiota and cellular compartments of brain: Implications for neurodevelopmental and neuropsychiatric disorders. Translational Psychiatry. 2025;15(1):278. DOI: https://doi.org/10.1038/s41398-025-03504-2. Mittal R, Debs LH, Patel AP, Nguyen D, Patel K, O’Connor G, et al. Neurotransmitters: The critical modulators regulating gut–brain axis. Journal of Cellular Physiology. 2017;232(9):2359–2372. DOI: https://doi.org/10.1002/jcp.25518. O’Riordan KJ, Moloney GM, Keane L, Clarke G, Cryan JF. The gut microbiota-immune-brain axis: Therapeutic implications. Cell Reports Medicine. 2025;6(3):101982. DOI: https://doi.org/10.1016/j.xcrm.2025.101982. Obrenovich M, Sankar Chittoor Mana T, Rai H, Shola D, Sass C, McCloskey B, et al. Recent findings within the microbiota–gut–brain–endocrine metabolic interactome. Pathology and Laboratory Medicine International. 2017;9:21–30. DOI: https://doi.org/10.2147/PLMI.S121487 Stilling RM, Van De Wouw M, Clarke G, Stanton C, Dinan TG, Cryan JF. The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis? Neurochemistry International. 2016;99:110–132. DOI: https://doi.org/10.1016/J.NEUINT.2016.06.011. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Science Translational Medicine. 2014;6(263):263ra158. DOI: https://doi.org/10.1126/scitranslmed.3009759. Jarman JB, Torres PJ, Stromberg S, Sato H, Stack C, Ladrillono A, et al. Bifidobacterium deficit in United States infants drives prevalent gut dysbiosis. Communications Biology. 2025;8(1):867. DOI: https://doi.org/10.1038/s42003-025-08274-7. Liang C, Zhang LW. Profiling the gut microbiota in obese children with formula feeding in early life and selecting strains against obesity. Foods. 2024;13(9):1379. DOI: https://doi.org/10.3390/foods13091379. Olbjørn C, Småstuen MC, Moen AE. Targeted analysis of the gut microbiome for diagnosis, prognosis and treatment individualization in pediatric inflammatory bowel disease. Microorganisms. 2022;10(7):1273. DOI: https://doi.org/10.3390/microorganisms10071273. Ojeda J, Ávila A, Vidal PM. Gut microbiota interaction with the central nervous system throughout life. Journal of Clinical Medicine. 2021;10(6):1299. DOI: https://doi.org/10.3390/jcm10061299. Andreo-Martínez P, Rubio-Aparicio M, Sanchez-Meca J, Veas A, Martínez-González AE. A meta-analysis of gut microbiota in children with autism. Journal of Autism and Developmental Disorders. 2022;52(3):1374–1387. DOI: https://doi.org/10.1007/s10803-021-05002-y. Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe. 2010;16(4):444–453. DOI: https://doi.org/10.1016/J.ANAEROBE.2010.06.008. De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A, Serrazzanetti DI, et al. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PloS One. 2013;8(10):e76993. DOI: https://doi.org/10.1371/journal.pone.0076993. Tomova A, Husarova V, Lakatosova S, Bakos J, Vlkova B, Babinska K, et al. Gastrointestinal microbiota in children with autism in Slovakia. Physiology & Behavior. 2015;138:179–187. DOI: https://doi.org/10.1016/J.PHYSBEH.2014.10.033. Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Applied and Environmental Microbiology. 2011;77(18):6718–6721. DOI: https://doi.org/10.1128/AEM.05212-11. Adams JB, Johansen LJ, Powell LD, Quig D, Rubin RA. Gastrointestinal flora and gastrointestinal status in children with autism — comparisons to typical children and correlation with autism severity. BMC Gastroenterology. 2011;11(1):22. DOI: https://doi.org/10.1186/1471-230X-11-22. Romano K, Shah AN, Schumacher A, Zasowski C, Zhang T, Bradley-Ridout G, et al. The gut microbiome in children with mood, anxiety, and neurodevelopmental disorders: An umbrella review. Gut Microbiome. 2023;4:e18. DOI: https://doi.org/10.1017/gmb.2023.16. Martín R, Bottacini F, Egan M, Chamignon C, Tondereau V, Moriez R, et al. The infant-derived Bifidobacterium bifidum strain CNCM I-4319 strengthens gut functionality. Microorganisms. 2020;8(9):1313. DOI: https://doi.org/10.3390/microorganisms8091313. Turroni F, Duranti S, Milani C, Lugli GA, van Sinderen D, Ventura M. Bifidobacterium bifidum: A key member of the early human gut microbiota. Microorganisms. 2019;7(11):544. DOI: https://doi.org/10.3390/microorganisms7110544. Wang LJ, Tsai CS, Chou WJ, Kuo HC, Huang YH, Lee SY, et al. Add-on Bifidobacterium bifidum supplement in children with attention-deficit/hyperactivity disorder: A 12-week randomized double-blind placebo-controlled clinical trial. Nutrients. 2024;16(14):2260. DOI: https://doi.org/10.3390/nu16142260. Ismail IH, Boyle RJ, Licciardi PV, Oppedisano F, Lahtinen S, Robins‐Browne RM, et al. Early gut colonization by Bifidobacterium breve and B. catenulatum differentially modulates eczema risk in children at high risk of developing allergic disease. Pediatric Allergy and Immunology. 2016;27(8):838–846. DOI: https://doi.org/10.1111/pai.12646. Aarts E, Ederveen TH, Naaijen J, Zwiers MP, Boekhorst J, Timmerman HM, et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PloS One. 2017;12(9):e0183509. DOI: https://doi.org/10.1371/journal.pone.0183509. Widdowson M, Shah S, Thorsen J, Poulsen CS, Rosenberg JB, Mohammadzadeh P, et al. Neonatal gut Bifidobacterium associates with indole-3-lactic acid levels in blood and risk of ADHD at age 10. Molecular Psychiatry. 2026;31:3544–3557. DOI: https://doi.org/10.1038/s41380-026-03480-z. Musilova S, Rada V, Marounek M, Nevoral J, Dušková D, Bunesova V, et al. Prebiotic effects of a novel combination of galactooligosaccharides and maltodextrins. Journal of Medicinal Food. 2015;18(6):685–689. DOI: https://doi.org/10.1089/jmf.2013.0187. Pokusaeva K, Fitzgerald GF, Van Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes & Nutrition. 2011;6(3):285–306. DOI: https://doi.org/10.1007/s12263-010-0206-6. Sugahara H, Odamaki T, Hashikura N, Abe F. Differences in folate production by bifidobacteria of different origins. Bioscience of Microbiota, Food and Health. 2015;34(4):87–93. DOI: https://doi.org/10.12938/bmfh.2015-003. Alessandri G, Ossiprandi MC, MacSharry J, van Sinderen D, Ventura M. Bifidobacterial dialogue with its human host and consequent modulation of the immune system. Frontiers in Immunology. 2019;10:2348. DOI: https://doi.org/10.3389/fimmu.2019.02348. Tatsiopoulou P, Serdari A, Bonti E, Zilikis N. Mental disorders in childhood and adolescence: A systematic review and meta-analysis of epidemiological data. BMC Psychiatry. 2025;25(1):1087. DOI: https://doi.org/10.1186/s12888-025-07532-6. Sacco R, Camilleri N, Eberhardt J, Umla-Runge K, Newbury-Birch D. A systematic review and meta-analysis on the prevalence of mental disorders among children and adolescents in Europe. European Child & Adolescent Psychiatry. 2024;33(9):2877–2894. DOI: https://doi.org/10.1007/s00787-022-02131-2. Njardvik U, Wergeland GJ, Riise EN, Hannesdottir DK, Öst LG. Psychiatric comorbidity in children and adolescents with ADHD: A systematic review and meta-analysis. Clinical Psychology Review. 2025;118:102571. DOI: https://doi.org/10.1016/j.cpr.2025.102571. Cryan JF, O’Riordan KJ, Cowan CS, Sandhu KV, Bastiaanssen TF, Boehme M, et al. The microbiota-gut-brain axis. Physiological Reviews. DOI: https://doi.org/10.1152/physrev.00018.2018. Jabbari Shiadeh SM, Chan WK, Rasmusson S, Hassan N, Joca S, Westberg L, et al. Bidirectional crosstalk between the gut microbiota and cellular compartments of brain: Implications for neurodevelopmental and neuropsychiatric disorders. Translational Psychiatry. 2025;15(1):278. DOI: https://doi.org/10.1038/s41398-025-03504-2. Mittal R, Debs LH, Patel AP, Nguyen D, Patel K, O’Connor G, et al. Neurotransmitters: The critical modulators regulating gut–brain axis. Journal of Cellular Physiology. 2017;232(9):2359–2372. DOI: https://doi.org/10.1002/jcp.25518. O’Riordan KJ, Moloney GM, Keane L, Clarke G, Cryan JF. The gut microbiota-immune-brain axis: Therapeutic implications. Cell Reports Medicine. 2025;6(3):101982. DOI: https://doi.org/10.1016/j.xcrm.2025.101982. Obrenovich M, Sankar Chittoor Mana T, Rai H, Shola D, Sass C, McCloskey B, et al. Recent findings within the microbiota–gut–brain–endocrine metabolic interactome. Pathology and Laboratory Medicine International. 2017;9:21–30. DOI: https://doi.org/10.2147/PLMI.S121487 Stilling RM, Van De Wouw M, Clarke G, Stanton C, Dinan TG, Cryan JF. The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis? Neurochemistry International. 2016;99:110–132. DOI: https://doi.org/10.1016/J.NEUINT.2016.06.011. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Science Translational Medicine. 2014;6(263):263ra158. DOI: https://doi.org/10.1126/scitranslmed.3009759. Jarman JB, Torres PJ, Stromberg S, Sato H, Stack C, Ladrillono A, et al. Bifidobacterium deficit in United States infants drives prevalent gut dysbiosis. Communications Biology. 2025;8(1):867. DOI: https://doi.org/10.1038/s42003-025-08274-7. Liang C, Zhang LW. Profiling the gut microbiota in obese children with formula feeding in early life and selecting strains against obesity. Foods. 2024;13(9):1379. DOI: https://doi.org/10.3390/foods13091379. Olbjørn C, Småstuen MC, Moen AE. Targeted analysis of the gut microbiome for diagnosis, prognosis and treatment individualization in pediatric inflammatory bowel disease. Microorganisms. 2022;10(7):1273. DOI: https://doi.org/10.3390/microorganisms10071273. Ojeda J, Ávila A, Vidal PM. Gut microbiota interaction with the central nervous system throughout life. Journal of Clinical Medicine. 2021;10(6):1299. DOI: https://doi.org/10.3390/jcm10061299. Andreo-Martínez P, Rubio-Aparicio M, Sanchez-Meca J, Veas A, Martínez-González AE. A meta-analysis of gut microbiota in children with autism. Journal of Autism and Developmental Disorders. 2022;52(3):1374–1387. DOI: https://doi.org/10.1007/s10803-021-05002-y. Finegold SM, Dowd SE, Gontcharova V, Liu C, Henley KE, Wolcott RD, et al. Pyrosequencing study of fecal microflora of autistic and control children. Anaerobe. 2010;16(4):444–453. DOI: https://doi.org/10.1016/J.ANAEROBE.2010.06.008. De Angelis M, Piccolo M, Vannini L, Siragusa S, De Giacomo A, Serrazzanetti DI, et al. Fecal microbiota and metabolome of children with autism and pervasive developmental disorder not otherwise specified. PloS One. 2013;8(10):e76993. DOI: https://doi.org/10.1371/journal.pone.0076993. Tomova A, Husarova V, Lakatosova S, Bakos J, Vlkova B, Babinska K, et al. Gastrointestinal microbiota in children with autism in Slovakia. Physiology & Behavior. 2015;138:179–187. DOI: https://doi.org/10.1016/J.PHYSBEH.2014.10.033. Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Applied and Environmental Microbiology. 2011;77(18):6718–6721. DOI: https://doi.org/10.1128/AEM.05212-11. Adams JB, Johansen LJ, Powell LD, Quig D, Rubin RA. Gastrointestinal flora and gastrointestinal status in children with autism — comparisons to typical children and correlation with autism severity. BMC Gastroenterology. 2011;11(1):22. DOI: https://doi.org/10.1186/1471-230X-11-22. Romano K, Shah AN, Schumacher A, Zasowski C, Zhang T, Bradley-Ridout G, et al. The gut microbiome in children with mood, anxiety, and neurodevelopmental disorders: An umbrella review. Gut Microbiome. 2023;4:e18. DOI: https://doi.org/10.1017/gmb.2023.16. Martín R, Bottacini F, Egan M, Chamignon C, Tondereau V, Moriez R, et al. The infant-derived Bifidobacterium bifidum strain CNCM I-4319 strengthens gut functionality. Microorganisms. 2020;8(9):1313. DOI: https://doi.org/10.3390/microorganisms8091313. Turroni F, Duranti S, Milani C, Lugli GA, van Sinderen D, Ventura M. Bifidobacterium bifidum: A key member of the early human gut microbiota. Microorganisms. 2019;7(11):544. DOI: https://doi.org/10.3390/microorganisms7110544. Wang LJ, Tsai CS, Chou WJ, Kuo HC, Huang YH, Lee SY, et al. Add-on Bifidobacterium bifidum supplement in children with attention-deficit/hyperactivity disorder: A 12-week randomized double-blind placebo-controlled clinical trial. Nutrients. 2024;16(14):2260. DOI: https://doi.org/10.3390/nu16142260. Ismail IH, Boyle RJ, Licciardi PV, Oppedisano F, Lahtinen S, Robins‐Browne RM, et al. Early gut colonization by Bifidobacterium breve and B. catenulatum differentially modulates eczema risk in children at high risk of developing allergic disease. Pediatric Allergy and Immunology. 2016;27(8):838–846. DOI: https://doi.org/10.1111/pai.12646. Aarts E, Ederveen TH, Naaijen J, Zwiers MP, Boekhorst J, Timmerman HM, et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PloS One. 2017;12(9):e0183509. DOI: https://doi.org/10.1371/journal.pone.0183509. Widdowson M, Shah S, Thorsen J, Poulsen CS, Rosenberg JB, Mohammadzadeh P, et al. Neonatal gut Bifidobacterium associates with indole-3-lactic acid levels in blood and risk of ADHD at age 10. Molecular Psychiatry. 2026;31:3544–3557. DOI: https://doi.org/10.1038/s41380-026-03480-z. Musilova S, Rada V, Marounek M, Nevoral J, Dušková D, Bunesova V, et al. Prebiotic effects of a novel combination of galactooligosaccharides and maltodextrins. Journal of Medicinal Food. 2015;18(6):685–689. DOI: https://doi.org/10.1089/jmf.2013.0187. Pokusaeva K, Fitzgerald GF, Van Sinderen D. Carbohydrate metabolism in Bifidobacteria. Genes & Nutrition. 2011;6(3):285–306. DOI: https://doi.org/10.1007/s12263-010-0206-6. Sugahara H, Odamaki T, Hashikura N, Abe F. Differences in folate production by bifidobacteria of different origins. Bioscience of Microbiota, Food and Health. 2015;34(4):87–93. DOI: https://doi.org/10.12938/bmfh.2015-003. Alessandri G, Ossiprandi MC, MacSharry J, van Sinderen D, Ventura M. Bifidobacterial dialogue with its human host and consequent modulation of the immune system. Frontiers in Immunology. 2019;10:2348. DOI: https://doi.org/10.3389/fimmu.2019.02348.