medsovetМедицинский СоветMeditsinskiy sovet = Medical Council2079-701X2658-5790REMEDIUM GROUP Ltd.10.21518/ms2024-304medsovet-8440Research ArticleПРАКТИКАPRACTICEОсобенности пристеночной и полостной кишечной микробиоты у детей первого года жизни, рожденных от матерей с бронхиальной астмой, в зависимости от способа родоразрешенияFeatures of the parietal and cavity intestinal microbiota in infants born to mothers with bronchial asthma, depending on the mode of deliveryhttps://orcid.org/0000-0002-6022-3420КосенковаТ. В.KosenkovaT. V.

Косенкова Тамара Васильевна, д.м.н., профессор, профессор кафедры детских болезней с клиникой Института медицинского образования

197341, Санкт- Петербург, ул. Аккуратова, д. 2

Tamara V. Kosenkova, Dr. Sci. (Med.), Professor, Professor of Children’s Diseases Department and Clinic of Institute of Medical Education

2, Akkuratov St., St Petersburg, 197341

tamara.kosenkova1955@gmail.comhttps://orcid.org/0000-0002-0992-1709НовиковаВ. П.NovikovaV. P.

Новикова Валерия Павловна, д.м.н., профессор, заведующий кафедрой пропедевтики детских болезней с курсом общего ухода за детьми, заведующий лабораторией «Медико-социальных проблем в педиатрии»

194100, Санкт-Петербург, ул. Литовская, д. 2

Valeriya P. Novikova, Dr. Sci. (Med.), Professor, Head of Department of Propaedeutics of Children’s Diseases with General Child Care Course, Head of Medical and Social Issues Laboratory

2, Litovskaya St., St Petersburg, 194100

novikova-vp@mail.ruhttps://orcid.org/0000-0001-8321-6162БойцоваЕ. А.BoytsovaE. A.

Бойцова Елена Александровна, аспирант кафедры детских болезней Института медицинского образования

197341, Санкт- Петербург, ул. Аккуратова, д. 2

Elena A. Boytsova, Postgraduate Student of Children’s Diseases Department and Clinic of Institute of Medical Education

2, Akkuratov St., St Petersburg, 197341

boitsova.e@gmail.comhttps://orcid.org/0000-0002-4449-2786КельмансонИ. А.KelmansonI. A.

Кельмансон Игорь Александрович, д.м.н., профессор, профессор кафедры детских болезней с клиникой Института медицинского образования

197341, Санкт- Петербург, ул. Аккуратова, д. 2

Igor A. Kelmanson, Dr. Sci. (Med.), Professor, Professor of Children’s Diseases Department and Clinic of Institute of Medical Education

2, Akkuratov St., St Petersburg, 197341

iakelmanson@hotmail.comhttps://orcid.org/0000-0003-4431-3917ЗазерскаяИ. Е.ZazerskayaI. E.

Зазерская Ирина Евгеньевна, д.м.н., профессор, заведующий кафедрой акушерства и гинекологии Института медицинского образования

197341, Санкт- Петербург, ул. Аккуратова, д. 2

Irina E. Zazerskaya, Dr. Sci. (Med.), Professor, Head of Department of Obstetrics and Gynecology, Institute of Medical Education

2, Akkuratov St., St Petersburg, 197341

zazera@mail.ruhttps://orcid.org/0000-0001-6827-1710ЛавроваО. В.LavrovaO. V.

 Лаврова Ольга Вольдемаровна, д.м.н., профессор, руководитель центра ранней диагностики аллергических заболеваний

197022, Санкт-Петербург, ул. Льва Толстого, д. 6–8

Olga V. Lavrova, Dr. Sci. (Med.), Professor, Head of Centre for Early Allergy Diagnosis

6–8, Lev Tolstoy St., St Petersburg, 197022

loverova@bk.ruhttps://orcid.org/0000-0003-2641-3471БолдыреваМ. Н.BoldyrevaM. N.

Болдырева Маргарита Николаевна, д.м.н., ведущий научный сотрудник лаборатории генетики гистосовместимости человека; медицинский директор

115478, Москва, Каширское шоссе, д. 24

117587, Москва, Варшавское шоссе, д. 125

Margarita N. Boldyreva, Dr. Sci. (Med.), Lead Research Associate, Human Histocompatibility Genetics Laboratory; Medical Director

24, Kashirskoye Shosse, Moscow, 115478

125, Varshavskoye Shosse, Moscow, 117587

boldyreva@dna-technology.ruНациональный медицинский исследовательский центр имени В.А. АлмазоваРоссияAlmazov National Medical Research CenterRussian FederationСанкт-Петербургский государственный педиатрический медицинский университетРоссияSt Petersburg State Pediatric Medical UniversityRussian FederationПервый Санкт-Петербургский государственный медицинский университет имени академика И.П. ПавловаРоссияPavlov First Saint Petersburg State Medical UniversityRussian FederationИнститут иммунологии; ДНК-ТехнологияРоссияInstitute of Immunology; DNA-Technology LLCRussian Federation202407082024011156–162Copyright © Косенкова Т.В., Новикова В.П., Бойцова Е.А., Кельмансон И.А., Зазерская И.Е., Лаврова О.В., Болдырева М.Н., 20242024Косенкова Т.В., Новикова В.П., Бойцова Е.А., Кельмансон И.А., Зазерская И.Е., Лаврова О.В., Болдырева М.Н.Kosenkova T.V., Novikova V.P., Boytsova E.A., Kelmanson I.A., Zazerskaya I.E., Lavrova O.V., Boldyreva M.N.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.med-sovet.pro/jour/article/view/8440Введение

Введение. Кишечная микробиота – сложная и уникальная по своему составу система, выполняющая в организме огромное количество разнообразных функций. Ее становление начинается еще внутриутробно.

Цель

Цель. Изучить особенности пристеночной и полостной кишечной микробиоты у детей, рожденных от матерей, страдающих бронхиальной астмой средней степени тяжести, в зависимости от способа родоразрешения.

Материалы и методы

Материалы и методы. Проведено проспективное лонгитудинальное исследование, в которое включались дети с первого дня жизни до 12 мес. Всего включено 68 детей с высоким риском развития атопии (HRA) от матерей с бронхиальной астмой, из которых 22 ребенка родились путем операции кесарева сечения и 46 – через естественные родовые пути. Качественный и количественный анализ кишечной микробиоты проводили методом реал-тайм ПЦР с группо- и видоспецифическими праймерами: у обследованных детей оценивалась динамика 4 филумов, включающих 31 микроорганизм. Забор кала ребенка и браш-биоптата из прямой кишки проводили в 7 контрольных точках измерения: в 1-е сут. после рождения и далее каждые 2 мес. до достижения ребенком возраста 1 года.

Результаты и обсуждение

Результаты и обсуждение. Полученные данные показали, что способ родоразрешения оказывает влияние на становление кишечной микробиоты: у детей, рожденных путем операции кесарева сечения, в пристеночной микробиоте, начиная с возраста 1–2, а в полостной – 3–4 мес., преобладающими микроорганизмами являлись представители филума Firmicutes (Clostridium leptum gr m.), в то время как у детей, рожденных через естественные родовые пути, все первые 8 мес. жизни в полостной и пристеночной микробиоте превалировали представители филума Bacteroidetes (Bacteroides spp., Prevotella spp.). Clostridium leptum может быть маркером воспалительного процесса в слизистой оболочке кишечника у детей с высоким риском атопии. Исследования последних лет показали, что Clostridium leptum способствует секреции противовоспалительных (IL-10 и IL-12) и ингибированию продукции провоспалительного (IL-8) цитокинов, а также увеличивает количество Treg-клеток.

Выводы

Выводы. Способ родоразрешения у детей с высоким риском атопии является дополнительным эпигенетическим фактором, который оказывает влияние на характер как пристеночной, так и полостной микробиоты.

Introduction

Introduction. Intestinal microbiota is a complex and unique system in its composition, performing a huge number of diverse functions in the body. Its formation begins in utero.

Aim

Aim. To study the features of the parietal and cavity intestinal microbiota in children born to mothers suffering from moderate bronchial asthma, depending on the mode of delivery.

Material and methods

Material and methods. A prospective longitudinal study was carried out, which included children from the first day of life to 12 months. A total of 68 children at high risk of atopy (HRA) from mothers with asthma were included, of whom 22 were born by cesarean section and 46 were born through the vaginal birth canal. Qualitative and quantitative analysis of GM was carried out by real-time PCR with group- and species-specific primers: in the examined children, the dynamics of 4 phylums including 31 microorganisms was assessed. The child’s feces and brush-biopsy were taken from the rectum at 7 control points of measurement.

Results and discussion

Results and discussion. The data obtained showed that the method of delivery has an impact on the formation of the intestinal microbiota: in children born by cesarean section, in the parietal microbiota, starting from the age of 1–2 months, and in the cavity microbiota – 3–4 months, representatives of phylum Firmicutes (Clostridium leptum gr m.). In children born through the vaginal birth canal, all the first 8 months of life in the cavity and parietal microbiota were dominated by representatives of phylum Bacteroidetes (Bacteroides spp., Prevotella spp.). Clostridium leptum can be a marker of an inflammatory process in the intestinal mucosa in children at high risk of atopy. The research conducted over the past few years has found that Clostridium leptum promotes the secretion of anti-inflammatory (IL-10 and IL-12) and inhibition of the production of pro-inflammatory (IL-8) cytokines, and also boosts the number of Treg cells.

Conclusion

Conclusion. The mode of delivery in children with a high risk of atopy is an additional epigenetic factor that influences the nature of both the parietal and cerebrospinal microbiota.

беременныебронхиальная астмадетикесарево сечениеестественное родоразрешениемикробиота кишечникаpregnant womenbronchial asthmachildrencesarean sectionnatural deliveryintestinal microbiotaReferencesЗахарова ИН, Османов ИМ, Бережная ИВ, Кольцов КА, Дедикова ОВ, Кучина АЕ и др. Кесарево сечение. Оправдан ли выбор? Риски для здоровья детей. Медицинский совет. 2018;(17):16–21. Режим доступа: https://www.med-sovet.pro/jour/article/view/2691.Zakharova IN, Osmanov IM, Berezhnaya IV, Koltsov KA, Dedikova OV, Kuchina AE et al. Cesarean section. Is the choice justified? Risks to children’s health. Meditsinskiy Sovet. 2018;(17):16–21 (In Russ.) Available at: https://www.med-sovet.pro/jour/article/view/2691.Лебеденко ЕЮ, Беспалая АВ, Феоктистова ТЕ, Рымашевский МА. Анализ мировых трендов уровня кесарева сечения с использованием классификации Робсона. Медицинский вестник Юга России. 2021;12(2):16–21. https://doi.org/10.21886/2219-8075-2021-12-2-16-21.Lebedenko EYu, Bespalaya AV, Feoktistova TE, Rymashevskiy MA. Analysis of global trends in caesarean section rates using the Robson classification. Medical Herald of the South of Russia. 2021;12(2):16–21. (In Russ.) https://doi.org/10.21886/2219-8075-2021-12-2-16-21.Lavin T, Preen DB. Investigating Caesarean Section Birth as a Risk Factor for Childhood Overweight. Child Obes. 2018;14(2):131–138. https://doi.org/10.1089/chi.2017.0034.Lavin T, Preen DB. Investigating Caesarean Section Birth as a Risk Factor for Childhood Overweight. Child Obes. 2018;14(2):131–138. https://doi.org/10.1089/chi.2017.0034.Wampach L, Heintz-Buschart A, Fritz JV, Ramiro-Garcia J, Habier J, Herold M et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat Commun. 2018;30;9(1):5091. https://doi.org/10.1038/s41467-018-07631-x.Wampach L, Heintz-Buschart A, Fritz JV, Ramiro-Garcia J, Habier J, Herold M et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat Commun. 2018;30;9(1):5091. https://doi.org/10.1038/s41467-018-07631-x.Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314–326. https://doi.org/10.1038/nm.4272.Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314–326. https://doi.org/10.1038/nm.4272.McDonnell L, Gilkes A, Ashworth M, Rowland V, Harries TH, Armstrong D, White P. Association between antibiotics and gut microbiome dysbiosis in children: systematic review and meta-analysis. Gut Microbes. 2021;13(1):1–18. https://doi.org/10.1080/19490976.2020.1870402.McDonnell L, Gilkes A, Ashworth M, Rowland V, Harries TH, Armstrong D, White P. Association between antibiotics and gut microbiome dysbiosis in children: systematic review and meta-analysis. Gut Microbes. 2021;13(1):1–18. https://doi.org/10.1080/19490976.2020.1870402.Kim H, Sitarik AR, Woodcroft K, Johnson CC, Zoratti E. Birth Mode, Breastfeeding, Pet Exposure, and Antibiotic Use: Associations With the Gut Microbiome and Sensitization in Children. Curr Allergy Asthma Rep. 2019;19(4):22. https://doi.org/10.1007/s11882-019-0851-9.Kim H, Sitarik AR, Woodcroft K, Johnson CC, Zoratti E. Birth Mode, Breastfeeding, Pet Exposure, and Antibiotic Use: Associations With the Gut Microbiome and Sensitization in Children. Curr Allergy Asthma Rep. 2019;19(4):22. https://doi.org/10.1007/s11882-019-0851-9.Henrick BM, Hutton AA, Palumbo MC, Casaburi G, Mitchell RD, Underwood MA et al. Elevated Fecal pH Indicates a Profound Change in the Breastfed Infant Gut Microbiome Due to Reduction of Bifidobacterium over the Past Century. mSphere. 2018;3(2):e00041-18. https://doi.org/10.1128/mSphere.00041-18.Henrick BM, Hutton AA, Palumbo MC, Casaburi G, Mitchell RD, Underwood MA et al. Elevated Fecal pH Indicates a Profound Change in the Breastfed Infant Gut Microbiome Due to Reduction of Bifidobacterium over the Past Century. mSphere. 2018;3(2):e00041-18. https://doi.org/10.1128/mSphere.00041-18.Бовбель ИЭ. Современные представления о микробиоте кишечника и возможности эффективного применения пробиотиков в практике врача-педиатра. Медицинские новости. 2017;(2):25–31. Режим доступа: https://cyberleninka.ru/article/n/sovremennye-predstavleniyaomikrobiote-kishechnika-i-vozmozhnostieffektivnogo-primeneniyaprobiotikovv-praktike-vracha-pediatra.Bovbel IE. Intestinal microbiota and use of probiotics in pediatric practice. Meditsinskie Novosti. 2017;(2):25–31. (In Russ.) Available at: https://cyberleninka.ru/article/n/sovremennye-predstavleniyao-mikrobiote-kishechnika-i-vozmozhnostieffektivnogo-primeneniya-probiotikovv-praktike-vracha-pediatra.Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016;16(1):86. https://doi.org/10.1186/s12876-016-0498-0.Rutayisire E, Huang K, Liu Y, Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: a systematic review. BMC Gastroenterol. 2016;16(1):86. https://doi.org/10.1186/s12876-016-0498-0.Kumar H, Collado MC, Wopereis H, Salminen S, Knol J, Roeselers G. The Bifidogenic Effect Revisited – Ecology and Health Perspectives of Bifidobacterial Colonization in Early Life. Microorganisms. 2020;8(12):1855. https://doi.org/10.3390/microorganisms8121855.Kumar H, Collado MC, Wopereis H, Salminen S, Knol J, Roeselers G. The Bifidogenic Effect Revisited – Ecology and Health Perspectives of Bifidobacterial Colonization in Early Life. Microorganisms. 2020;8(12):1855. https://doi.org/10.3390/microorganisms8121855.Akagawa S, Kaneko K. Gut microbiota and allergic diseases in children. Allergol Int. 2022;71(3):301–309. https://doi.org/10.1016/j.alit.2022.02.004.Akagawa S, Kaneko K. Gut microbiota and allergic diseases in children. Allergol Int. 2022;71(3):301–309. https://doi.org/10.1016/j.alit.2022.02.004.Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol. 2013;208(3):226. https://doi.org/10.1016/j.ajog.2013.01.018.Stout MJ, Conlon B, Landeau M, Lee I, Bower C, Zhao Q et al. Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am J Obstet Gynecol. 2013;208(3):226. https://doi.org/10.1016/j.ajog.2013.01.018.Pandey PK, Verma P, Kumar P, Bavdekar B, Patole MS, Shouche YS. Comparative analysis of fecal microflora of healthy full-term Indian infants born with different methods of delivery (vaginal vs cesarean): Acinetobacter sp. prevalence in vaginally born infants. J Biosci. 2012;37(6):989–998. https://doi.org/0.1007/s12038-012-9268-5.Pandey PK, Verma P, Kumar P, Bavdekar B, Patole MS, Shouche YS. Comparative analysis of fecal microflora of healthy full-term Indian infants born with different methods of delivery (vaginal vs cesarean): Acinetobacter sp. prevalence in vaginally born infants. J Biosci. 2012;37(6):989–998. https://doi.org/0.1007/s12038-012-9268-5.Koren O, Konnikova L, Brodin P, Mysorekar IU, Collado MC. The maternal gut microbiome in pregnancy: implications for the developing immune system. Nat Rev Gastroenterol Hepatol. 2024;21(1):35–45. https://doi.org/10.1038/s41575-023-00864-2.Koren O, Konnikova L, Brodin P, Mysorekar IU, Collado MC. The maternal gut microbiome in pregnancy: implications for the developing immune system. Nat Rev Gastroenterol Hepatol. 2024;21(1):35–45. https://doi.org/10.1038/s41575-023-00864-2.Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–117. https://doi.org/10.1016/j.molmed.2014.12.002.Mueller NT, Bakacs E, Combellick J, Grigoryan Z, Dominguez-Bello MG. The infant microbiome development: mom matters. Trends Mol Med. 2015;21(2):109–117. https://doi.org/10.1016/j.molmed.2014.12.002.Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T et al. Motherto-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS ONE. 2013;8(11):e78331. https://doi.org/10.1371/journal.pone.0078331.Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T et al. Motherto-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PLoS ONE. 2013;8(11):e78331. https://doi.org/10.1371/journal.pone.0078331.Betran AP, Torloni MR, Zhang JJ, Gulmezoglu AM. WHO Statement on Caesarean Section Rates. BJOG. 2016;123(5):667–670. https://doi.org/10.1111/1471-0528.13526.Betran AP, Torloni MR, Zhang JJ, Gulmezoglu AM. WHO Statement on Caesarean Section Rates. BJOG. 2016;123(5):667–670. https://doi.org/10.1111/1471-0528.13526.Reyman M, van Houten MA, van Baarle D, Bosch AATM, Man HW, Chu MLJN et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;0(1):4997. https://doi.org/10.1038/s41467-019-13014-7.Reyman M, van Houten MA, van Baarle D, Bosch AATM, Man HW, Chu MLJN et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;0(1):4997. https://doi.org/10.1038/s41467-019-13014-7.Dominguez-Bello MG, Costello EK, 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(26):11971–11975. https://doi.org/10.1073/pnas.1002601107.Dominguez-Bello MG, Costello EK, 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(26):11971–11975. https://doi.org/10.1073/pnas.1002601107.Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB et al. Roles of Birth Mode and Infant Gut Microbiota in Intergenerational Transmission of Overweight and Obesity From Mother to Offspring. JAMA Pediatr. 2018;172(4):368–377. https://doi.org/10.1001/jamapediatrics.2017.5535.Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB et al. Roles of Birth Mode and Infant Gut Microbiota in Intergenerational Transmission of Overweight and Obesity From Mother to Offspring. JAMA Pediatr. 2018;172(4):368–377. https://doi.org/10.1001/jamapediatrics.2017.5535.Zhang T, Sidorchuk A, Sevilla-Cermeno L, Vilaplana-Perez A, Chang Z, Larsson H, Mataix-Cols D, Fernandez de la Cruz L. Association of Cesarean Delivery With Risk of Neurodevelopmental and Psychiatric Disorders in the Offspring: A Systematic Review and Meta-analysis. JAMA Netw Open. 2019;2(8):e1910236. https://doi.org/10.1001/jamanetworkopen.2019.10236.Zhang T, Sidorchuk A, Sevilla-Cermeno L, Vilaplana-Perez A, Chang Z, Larsson H, Mataix-Cols D, Fernandez de la Cruz L. Association of Cesarean Delivery With Risk of Neurodevelopmental and Psychiatric Disorders in the Offspring: A Systematic Review and Meta-analysis. JAMA Netw Open. 2019;2(8):e1910236. https://doi.org/10.1001/jamanetworkopen.2019.10236.Curran EA, O’Neill SM, Cryan JF, Kenny LC, Dinan TG, Khashan AS, Kearney PM. Research review: Birth by caesarean section and development of autism spectrum disorder and attention-deficit/hyperactivity disorder: A systematic review and meta-analysis. J Child Psychol Psychiatry. 2015;56(5):500–508. https://doi.org/10.1111/jcpp.12351.Curran EA, O’Neill SM, Cryan JF, Kenny LC, Dinan TG, Khashan AS, Kearney PM. Research review: Birth by caesarean section and development of autism spectrum disorder and attention-deficit/hyperactivity disorder: A systematic review and meta-analysis. J Child Psychol Psychiatry. 2015;56(5):500–508. https://doi.org/10.1111/jcpp.12351.Stokholm J, Thorsen J, Chawes BL, Schjorring S, Krogfelt KA, Bonnelykke K, Bisgaard H. Cesarean section changes neonatal gut colonization. J Allergy Clin Immunol. 2016;138(3):881–889.e2. https://doi.org/10.1016/j.jaci.2016.01.028.Stokholm J, Thorsen J, Chawes BL, Schjorring S, Krogfelt KA, Bonnelykke K, Bisgaard H. Cesarean section changes neonatal gut colonization. J Allergy Clin Immunol. 2016;138(3):881–889.e2. https://doi.org/10.1016/j.jaci.2016.01.028.Polos J, Flatcher J. Caesarean section and children’s health: A quasi-experimental design. Popul Stud. 2019;73(3):353–368. https://doi.org/10.1080/00324728.2019.1624810.Polos J, Flatcher J. Caesarean section and children’s health: A quasi-experimental design. Popul Stud. 2019;73(3):353–368. https://doi.org/10.1080/00324728.2019.1624810.Dubois L, Valles-Colomer M, Ponsero A, Helve O, Andersson S, Kolho KL et al. Paternal and induced gut microbiota seeding complement mother-to-infant transmission. Cell Host Microbe. 2024;32(6):1011–1024.e4. https://doi.org/10.1016/j.chom.2024.05.004.Dubois L, Valles-Colomer M, Ponsero A, Helve O, Andersson S, Kolho KL et al. Paternal and induced gut microbiota seeding complement mother-to-infant transmission. Cell Host Microbe. 2024;32(6):1011–1024.e4. https://doi.org/10.1016/j.chom.2024.05.004.Kuziel GA, Rakoff-Nahoum S. The gut microbiome. Curr Biol. 2022;32(6):R257-R264. https://doi.org/10.1016/j.cub.2022.02.023.Kuziel GA, Rakoff-Nahoum S. The gut microbiome. Curr Biol. 2022;32(6):R257-R264. https://doi.org/10.1016/j.cub.2022.02.023.Neu J. Dysbiosis in the Neonatal Period: Role of Cesarean Section. Nestle Nutr Inst Workshop Ser. 2017;88:57–66. https://doi.org/10.1159/000455215.Neu J. Dysbiosis in the Neonatal Period: Role of Cesarean Section. Nestle Nutr Inst Workshop Ser. 2017;88:57–66. https://doi.org/10.1159/000455215.Derrien M, Alvarez AS, de Vos WM. The Gut Microbiota in the First Decade of Life. Trends Microbiol. 2019;27(12):997–1010. https://doi.org/10.1016/j.tim.2019.08.001.Derrien M, Alvarez AS, de Vos WM. The Gut Microbiota in the First Decade of Life. Trends Microbiol. 2019;27(12):997–1010. https://doi.org/10.1016/j.tim.2019.08.001.Gao Y, Nanan R, Macia L, Tan J, Sominsky L, Quinn TP et al. The maternal gut microbiome during pregnancy and offspring allergy and asthma. J Allergy Clin Immunol. 2021;148(3):669–678. https://doi.org/10.1016/j.jaci.2021.07.011.Gao Y, Nanan R, Macia L, Tan J, Sominsky L, Quinn TP et al. The maternal gut microbiome during pregnancy and offspring allergy and asthma. J Allergy Clin Immunol. 2021;148(3):669–678. https://doi.org/10.1016/j.jaci.2021.07.011.Lee HL, Shen H, Hwang IY, Ling H, Yew WS, Lee YS, Chang MW. Targeted Approaches for in situ gut microbiome manipulation. Genes (Basel). 2018;9(7):351. https://doi.org/10.3390/genes9070351.Lee HL, Shen H, Hwang IY, Ling H, Yew WS, Lee YS, Chang MW. Targeted Approaches for in situ gut microbiome manipulation. Genes (Basel). 2018;9(7):351. https://doi.org/10.3390/genes9070351.Grech A, Collins CE, Holmes A, Lal R, Duncanson K, Taylor R, Gordon A. Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis. Gut Microbes. 2021;13(1):1–30. https://doi.org/10.1080/19490976.2021.1897210.Grech A, Collins CE, Holmes A, Lal R, Duncanson K, Taylor R, Gordon A. Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis. Gut Microbes. 2021;13(1):1–30. https://doi.org/10.1080/19490976.2021.1897210.Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. https://doi.org/10.1038/s41586-019-1560-1.Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. https://doi.org/10.1038/s41586-019-1560-1.Chawla M, Gupta R, Das B. Gut microbiome dysbiosis in malnutrition. Prog Mol Biol Transl Sci. 2022;192(1):205–229. https://doi.org/10.1016/bs.pmbts.2022.07.011.Chawla M, Gupta R, Das B. Gut microbiome dysbiosis in malnutrition. Prog Mol Biol Transl Sci. 2022;192(1):205–229. https://doi.org/10.1016/bs.pmbts.2022.07.011.Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703. https://doi.org/10.1016/j.chom.2015.04.004.Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(5):690–703. https://doi.org/10.1016/j.chom.2015.04.004.MacIntyre DA, Chandiramani M, Lee YS, Kindinger L, Smith A, Angelopoulos N et al. The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci Rep. 2015;5:8988. https://doi.org/10.1038/srep08988.MacIntyre DA, Chandiramani M, Lee YS, Kindinger L, Smith A, Angelopoulos N et al. The vaginal microbiome during pregnancy and the postpartum period in a European population. Sci Rep. 2015;5:8988. https://doi.org/10.1038/srep08988.Горелов АВ, Каннер ЕВ, Максимов МЛ, Ермолаева АС, Вознесенская АА, Дадашева КН. Кишечная микробиота: современные доказательные данные эффективности применения Lactobacillus rhamnosus GG и Bifidobacterium longum в практике педиатра. Медицинский совет. 2018;(11):175–180. https://doi.org/10.21518/2079-701X-2018-11-175-180.Gorelov AV, Kanner EV, Maximov ML, Ermolaeva AS, Voznesenskaya AA, Dadasheva KN. Intestinal microbiota: updated evidence-based data on the efficacy of Lactobacillus rhamnosus GG and Bifidobacterium longum in pediatric practice. Meditsinskiy Sovet. 2018;(11):175–180. (In Russ.) https://doi.org/10.21518/2079-701X-2018-11-175-180.Страхова СС, Самоукина АМ, Алексеева ЮА, Родионов АА, Страхов МА. Микроэкологические биомаркеры уровня резистентности организма у новорожденных детей. Медицина. 2022;10(3):63–71. https://doi.org/10.29234/2308-9113-2022-10-3-63-71.Strahova SS, Samoukina AM, Alekseeva UA, Rodionov AA, Strahov MA. Microecological biomarkers of the level of body resistance in newborns. Medicine. 2022;10(3):63–71. (In Russ.) https://doi.org/10.29234/23089113-2022-10-3-63-71.Šumilo D, Nirantharakumar K, Willis BH, Rudge GM, Martin J, Gokhale K et al. Long-term impact of pre-incision antibiotics on children born by caesarean section: a longitudinal study based on UK electronic health records. Health Technol Assess. 2022;26(30):1–160. https://doi.org/10.3310/ZYZC8514.Šumilo D, Nirantharakumar K, Willis BH, Rudge GM, Martin J, Gokhale K et al. Long-term impact of pre-incision antibiotics on children born by caesarean section: a longitudinal study based on UK electronic health records. Health Technol Assess. 2022;26(30):1–160. https://doi.org/10.3310/ZYZC8514.Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(05):690–703. https://doi.org/10.1016/j.chom.2015.04.004.Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015;17(05):690–703. https://doi.org/10.1016/j.chom.2015.04.004.Nagpal R, Tsuji H, Takahashi T, Nomoto K, Kawashima K, Nagata S, Yamashiro Y. Gut dysbiosis following C-section instigates higher colonisation of toxigenic Clostridium perfringens in infants. Benef Microbes. 2017;8(3):353–365. https://doi.org/10.3920/BM2016.0216.Nagpal R, Tsuji H, Takahashi T, Nomoto K, Kawashima K, Nagata S, Yamashiro Y. Gut dysbiosis following C-section instigates higher colonisation of toxigenic Clostridium perfringens in infants. Benef Microbes. 2017;8(3):353–365. https://doi.org/10.3920/BM2016.0216.Янковский ДС, Антипкин ЮГ, Дымент ГС, Знаменская ТК, Шунько ЕЕ, Давыдова ЮВ. Микробная экология новорожденных: особенности формирования микробиома и профилактика его нарушений. Неонатологія, хірургія та перинатальна медицина. 2015;5(2):93–105. Режим доступа: https://www.researchgate.net/publication/328425982_MICROBE_ECOLOGY_OF_NEONATES_SPECIFICS_OF_MICROBIOME_FORMATION_AND_PROPHYLAXES_OF_ITS_DISORDERS.Yankovskiy DS, Antipkin YuG, Dyment GS, Znamenskaia TK, Shunko EE, Davydova Yu V. Microbe ecology of neonates: specifics of microbiome formation and prophylaxes of its disorders Neonatology Surgery and Perinatal Medicine. 2015;5(2):93–105. (In Russ.) Available at: https://www.researchgate.net/publication/328425982_MICROBE_ECOLOGY_OF_NEONATES_SPECIFICS_OF_MICROBIOME_FORMATION_AND_PROPHYLAXES_OF_ITS_DISORDERS.Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82. https://doi.org/10.1126/scitranslmed.aad7121.Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med. 2016;8(343):343ra82. https://doi.org/10.1126/scitranslmed.aad7121.Самоукина АМ, Алексеева ЮА, Страхова СС, Страхов МА. Особенности микробиоты недоношенных новорожденных с дефицитом массы тела. Экспериментальная и клиническая гастроэнтерология. 2022;(4):78–86. https://doi.org/10.31146/1682-8658-ecg-200-4-78-86Samoukina AM, Alekseeva UA, Strakhova SS, Strakhov MA. Features of microbiota in underweight premature infants. Experimental and Clinical Gastroenterology. 2022;(4):78–86. (In Russ.) https://doi.org/10.31146/16828658-ecg-200-4-78-86.Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. https://doi.org/10.1038/s41586019-1560-1.Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. https://doi.org/10.1038/s41586019-1560-1.Andersen V, Moller S, Jensen PB, Moller FT, Green A. Caesarean delivery and risk of chronic inflammatory diseases (Inflammatory bowel disease, rheumatoid arthritis, coeliac disease, and diabetes mellitus): a population based registry study of 2,699,479 births in Denmark during 1973–2016. Clin Epidemiol. 2020;12:287–293. https://doi.org/10.2147/CLEP.S229056.Andersen V, Moller S, Jensen PB, Moller FT, Green A. Caesarean delivery and risk of chronic inflammatory diseases (Inflammatory bowel disease, rheumatoid arthritis, coeliac disease, and diabetes mellitus): a population based registry study of 2,699,479 births in Denmark during 1973–2016. Clin Epidemiol. 2020;12:287–293. https://doi.org/10.2147/CLEP.S229056.Nazmul Huda M, Lewis Z, Kalanetra KM, Rashid M, Ahmad SM, Raqib R et al. Stool microbiota and vaccine responsesof infants. Pediatrics. 2014;134(2):e362–372. https://doi.org/10.1542/peds.2013-3937.Nazmul Huda M, Lewis Z, Kalanetra KM, Rashid M, Ahmad SM, Raqib R et al. Stool microbiota and vaccine responsesof infants. Pediatrics. 2014;134(2):e362–372. https://doi.org/10.1542/peds.2013-3937.Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestineimportant to infants’ and children’s health? J Pediatr Gastroenterol Nutr. 2015;60(3):294–307. https://doi.org/10.1097/MPG.0000000000000597.Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestineimportant to infants’ and children’s health? J Pediatr Gastroenterol Nutr. 2015;60(3):294–307. https://doi.org/10.1097/MPG.0000000000000597.Avershina E, Rubio CR, Lundgård K, Martinez GP, Collado MC, Storrø O, Øien et al. Effect of probiotics in prevention of atopic dermatitis is dependent on the intrinsic microbiota at early infancy. J Allergy Clin Immunol. 2017;139(4):1399–1402.e8. https://doi.org/10.1016/j.jaci.2016.09.056.Avershina E, Rubio CR, Lundgård K, Martinez GP, Collado MC, Storrø O, Øien et al. Effect of probiotics in prevention of atopic dermatitis is dependent on the intrinsic microbiota at early infancy. J Allergy Clin Immunol. 2017;139(4):1399–1402.e8. https://doi.org/10.1016/j.jaci.2016.09.056.Collado MC, Rautava S, Aakko J, Isolauri E, Salminen S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;(6):23129. https://doi.org/10.1038/srep23129.Collado MC, Rautava S, Aakko J, Isolauri E, Salminen S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;(6):23129. https://doi.org/10.1038/srep23129.Perez-Muñoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017;5(1):48. https://doi.org/10.1186/s40168-017-0268-4.Perez-Muñoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome. Microbiome. 2017;5(1):48. https://doi.org/10.1186/s40168-017-0268-4.Косенкова ТВ, Бойцова ЕА, Кельмансон ИА, Зазерская ИЕ, Новикова ВП, Лаврова ОВ и др. Пристеночная и полостная кишечная микробиота у детей первого года жизни, рожденных от матерей с бронхиальной астмой. Вопросы детской диетологии. 2022;20(4):5–20. https://doi.org/10.20953/1727-5784-2022-4-5-20.Kosenkova TV, Boitsova EA, Kelmanson IA, Zazerskay IE, Novikova VP, Lavrova OV et al. Luminal and mucosal-associated intestinal microbiota in children born to mothers with bronchial asthma during the first year of life. Pediatric Nutrition. 2022;20(4):5–20. (In Russ.) https://doi.org/10.20953/1727-5784-2022-4-5-20.Николаева ИВ, Царегородцев АД, Шайхиева ГС. Формирование кишечной микробиоты ребенка и факторы, влияющие на этот процесс. Российский вестник перинатологии и педиатрии. 2018;63:(3):13–18. https://doi.org/10.21508/1027-4065-2018-63-3-13-18.Nikolaeva IV, Tsaregorodtsev AD, Shaikhieva GS. Formation of the intestinal microbiota of children and the factors influence this process. Russian Bulletin of Perinatology and Pediatrics. 2018;63:(3):13–18. (In Russ.) https://doi.org/10.21508/1027-4065-2018-63-3-13-18.Hansen R, Scott KP, Khan S, Martin J, Berry SH, Stevenson M et al. First-Pass Meconium Samples from Healthy Term Vaginally-Delivered Neonates: An Analysis of the Microbiota. PLoS ONE. 2015;10(7):е0133320. https://doi.org/10.1371/journal.pone.0133320.Hansen R, Scott KP, Khan S, Martin J, Berry SH, Stevenson M et al. First-Pass Meconium Samples from Healthy Term Vaginally-Delivered Neonates: An Analysis of the Microbiota. PLoS ONE. 2015;10(7):е0133320. https://doi.org/10.1371/journal.pone.0133320.Navarro DJ, Foxcroft DR. Learning statistics with jamovi: a tutorial for psychology students and other beginners. 2022. https://doi.org/10.24384/hgc3-7p15.Navarro DJ, Foxcroft DR. Learning statistics with jamovi: a tutorial for psychology students and other beginners. 2022. https://doi.org/10.24384/hgc3-7p15.Ellis PD. The essential guide to effect sizes: statistical power, meta-analysis, and the interpretation of research results. NY: Cambridge University Press; 2010. 173 p. https://doi.org/10.1017/CBO9780511761676Ellis PD. The essential guide to effect sizes: statistical power, meta-analysis, and the interpretation of research results. NY: Cambridge University Press; 2010. 173 p. https://doi.org/10.1017/CBO9780511761676Hua ng F, Zhang Y, Bai XQ, Wang CX, Li YN. Clostridium leptum induces the generation of interleukin-10(+) regulatory B cells to alleviate airway inflammation in asthma. Mol Immunol. 2022;145:124–138. https://doi.org/10.1016/j.molimm.2022.03.010.Hua ng F, Zhang Y, Bai XQ, Wang CX, Li YN. Clostridium leptum induces the generation of interleukin-10(+) regulatory B cells to alleviate airway inflammation in asthma. Mol Immunol. 2022;145:124–138. https://doi.org/10.1016/j.molimm.2022.03.010.Huang F, Qiao H-M, Yin J-N, Gao Y, Ju Y-H, Li Y-N. Early-Life Exposure to Clostridium leptum. Causes Pulmonary Immunosuppression. PLoS ONE. 2015;10(11):e0141717. https://doi.org/10.1371/journal.pone.0141717Huang F, Qiao H-M, Yin J-N, Gao Y, Ju Y-H, Li Y-N. Early-Life Exposure to Clostridium leptum. Causes Pulmonary Immunosuppression. PLoS ONE. 2015;10(11):e0141717. https://doi.org/10.1371/journal.pone.0141717

The authors declare that there are no conflicts of interest present.