Changes in the microbiota of the upper airways and intestine in the treatment of acute respiratory infections in preschool children
https://doi.org/10.46563/1560-9561-2023-26-2-95-101
EDN: sylbld
Abstract
Introduction. The microbiota of the upper airways and intestine in preschool children is directly involved in protecting the growing body from acute respiratory infections (ARI), which are the most common infections in children, about 65% of them turn into recurrent respiratory infections (RRI). Aim. To establish changes in the microbiota of the upper airways and intestine in the treatment of ARI in preschool children.
Materials and methods. The study involved sixty 1–6 year (Me = 3.38 years) frequently ill children. They were divided into 3 groups depending on the chosen treatment lasting 90 days. Children of group 1 (n = 20) underwent nutrition correction. Children of group 2 (n = 20) received additional probiotics. Children of group 3 (n = 20) received both nutritional correction and probiotics at the prescribed doses. Before and after treatment, the composition of the microbiota of the oropharyngeal zone and intestine was determined by genetic sequencing of the V3–V4 region of the 16S ribosomal RNA gene, followed by bioinformatic analysis.
Results. Significant differences were found mainly in the relative content of Firmicutes in the microbiota of patients treated. The content of Firmicutes in the microbiota of children receiving probiotics against the background of nutrition correction (30%) was significantly higher than in patients with nutrition correction (26.91%) and in children receiving only probiotics (25.95%). In patients of different groups, after treatment, a decrease in the content of Proteobacteria in the microbiota of the oropharyngeal zone was revealed. A significant decrease in the relative content of Bacteroidota (by more than 3 times) in 95% of patients, and a decrease in Proteobacteria (by more than 4.5 times) in 100% of patients was also found in the intestinal microbiota of group 3 patients treated with probiotics. In addition, there was a significant increase in the Firmicutes microbiota from 21.97% to 30.07% in 85% of patients, and an increase in the content of Actinobacteriota from 1.9% to 5.7% in 95% of patients. The relative content of undifferentiated microbiota after therapy was also significantly higher (70.08%) than before treatment (58.40%) in 85% of patients.
Contribution:
Krasnorutskaya O.N., Kurdyukova T.I. — research concept and design of the study;
Kurdyukova T.I., Bugrimov D.Yu., Shevtsov A.N. — collection and processing of material;
Kurdyukova T.I. — statistical processing;
Kurdyukova T.I., Krasnorutskaya O.N. — text writing;
Krasnorutskaya O.N., Bugrimov D.Yu., Shevtsov A.N. — editing.
All co-authors — approval of the final version of the article, responsibility for the integrity of all parts of the article.
Acknowledgment. The study had no sponsorship.
Conflict of interest. The authors declare no conflict of interest.
Received: February 17, 2023
Accepted: March 21, 2023
Published: April 28, 2023
About the Authors
Tatiana I. KurdyukovaRussian Federation
MD, PhD student of the department of faculty and palliative pediatrics of the Voronezh State Medical University named after N.N. Burdenko of the Ministry of Health of the Russian Federation, Voronezh, 394036, Russian Federation
e-mail: tatuzya@yandex.ru
Olga N. Krasnorutskaya
Russian Federation
Daniil Yu. Bugrimov
Russian Federation
Artem N. Shevtsov
Russian Federation
References
1. Williams B.G., Gouws E., Boschi-Pinto C., Bryce J., Dye C. Estimates of world-wide distribution of child deaths from acute respiratory infections. Lancet Infect. Dis. 2002; 2(1): 25–32. https://doi.org/10.1016/s1473-3099(01)00170-0
2. Esposito S., Principi N. Impact of nasopharyngeal microbiota on the development of respiratory tract diseases. Eur. J. Clin. Microbiol. Infect. Dis. 2018; 37(1): 1–7. https://doi.org/10.1007/s10096-017-3076-7
3. Esposito S., Ballarini S., Argentiero A., Ruggiero L., Rossi G.A., Principi N. Microbiota profiles in pre-school children with respiratory infections: Modifications induced by the oral bacterial lysate OM-85. Front. Cell. Infect. Microbiol. 2022; 12: 789436. https://doi.org/10.3389/fcimb.2022.789436
4. Li Ya., Fu X., Ma J., Zhang J., Hu Yi, Dong W., et al. Altered respiratory virome and serum cytokine profile associated with recurrent respiratory tract infections in children. Nat. Commun. 2019; 10(1): 2288. https://doi.org/10.1038/s41467-019-10294-x
5. Rossi G.A., Pohunek P., Feleszko W., Ballarini S., Colin A.A. Viral infections and wheezing-asthma inception in childhood: is there a role for immunomodulation by oral bacterial lysates? Clin. Transl. Allergy. 2020; 10: 17. https://doi.org/10.1186/s13601-020-00322-1
6. Bogaert D., Keijser B., Huse S., Rossen J., Veenhoven R., van Gils E., et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PLoS One. 2011; 6(2): e17035. https://doi.org/10.1371/journal.pone.0017035
7. Hufnagl K., Pali-Schöll I., Roth-Walter F., Jensen-Jarolim E. Dysbiosis of the gut and lung microbiome has a role in asthma. Semin. Immunopathol. 2020; 42(1): 75–93. https://doi.org/10.1007/s00281-019-00775-y
8. Grandinetti R., Fainardi V., Caffarelli C., Capoferri G., Lazzara A., Tornesello M., et al. Risk factors affecting development and persistence of preschool wheezing: consensus document of the Emilia-Romagna Asthma (ERA) study group. J. Clin. Med. 2022; 11(21): 6558. https://doi.org/10.3390/jcm11216558
9. Nikolaeva I.V., Tsaregorodtsev A.D., Shaykhieva G.S. Formation of the intestinal microbiota of children and the factors that influence this process. Rossiyskiy vestnik perinatologii i pediatrii. 2018; 63(3): 13–8. https://doi.org/10.21508/1027-4065-2018-63-3-1318 https://elibrary.ru/xrhvcp (in Russian)
10. Smirnova G.I., Mankute G.R. Intestinal microbiota and atopic dermatitis in children. Rossiyskiy pediatricheskiy zhurnal. 2015; 18(6): 46–53. https://elibrary.ru/vkgooj (in Russian)
11. Smirnova G.I., Korsunskiy A.A. Disorders of skin microbiota and formation of atopic dermatitis in children. Rossiyskiy pediatricheskiy zhurnal. 2019; 22(4): 243–50. https://doi.org/10.18821/1560-9561-2019-22-4-243-250 https://elibrary.ru/ewyrkl (in Russian)
12. Kaul D., Rathnasinghe R., Ferres M. Microbiome disturbance and resilience dynamics of the upper respiratory tract during influenza A virus infection. Nat. Commun. 2020; 11(1): 2537. https://doi.org/10.1038/s41467-020-16429-9
13. Lloyd C.M., Marsland B.J. Lung homeostasis: influence of age, microbes, and the immune system. Immunity. 2017; 46(4): 549–61. https://doi.org/10.1016/j.immuni.2017.04.005
14. Cornick S., Tawiah A., Chadee K. Roles and regulation of the mucus barrier in the gut. Tissue Barriers. 2015; 3(1-2): e982426. https://doi.org10.4161/21688370.2014.982426
15. Kozlov I.G. Microbiota, mucosal immunity and antibiotics: the fineness of the interaction. Russkiy meditsinskiy zhurnal. 2018; 26(8-1): 19–27. https://elibrary.ru/maemlz (in Russian)
16. Song E.J., Lee E.S., Nam Y.D. Progress of analytical tools and techniques for human gut microbiome research. J. Microbiol. 2018; 56(10): 693–705. https://doi.org/10.1007/s12275-018-8238-5
17. Kwa W.T., Sundarajoo S., Toh K.Y., Lee J. Application of emerging technologies for gut microbiome research. Singapore Med. J. 2023; 64(1): 45–52. https://doi.org/10.4103/singaporemedj.SMJ-2021-432
18. Ibañez-Lligoña M., Colomer-Castell S., González-Sánchez A., Gregori J., Campos C., Garcia-Cehic D., et al. Bioinformatic tools for NGS-based metagenomics to improve the clinical diagnosis of emerging, re-emerging and new viruses. Viruses. 2023; 15(2): 587. https://doi.org/10.3390/v15020587
19. Schlaeppi K., Bulgarelli D. The plant microbiome at work. Mol. Plant Microbe Interact. 2015; 28(3): 212–7. https://doi.org/10.1094/MPMI-10-14-0334-FI
20. Lloyd-Price J., Abu-Ali G., Huttenhower C. The healthy human microbiome. Genome Med. 2016; 8(1): 51. https://doi.org/10.1186/s13073-016-0307-y
21. Ahrodia T., Das S., Bakshi S., Das B. Structure, functions, and diversity of the healthy human microbiome. Prog. Mol. Biol. Transl. Sci. 2022; 191(1): 53–82. https://doi.org/10.1016/bs.pmbts.2022.07.003
22. Anderson B.D., Bisanz J.E. Challenges and opportunities of strain diversity in gut microbiome research. Front. Microbiol. 2023; 14: 1117122. https://doi.org/10.3389/fmicb.2023.1117122
23. Rajilić-Stojanović M., de Vos W.M. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol. Rev. 2014; 38(5): 996–1047. https://doi.org/10.1111/1574-6976.12075
24. Lagier J.C., Million M., Hugon P., Armougom F., Raoult D. Human gut microbiota: repertoire and variations. Front. Cell. Infect. Microbiol. 2012; 2: 136. https://doi.org/10.3389/fcimb.2012.00136
25. Lagier J.C., Armougom F., Million M., Hugon P., Pagnier I., Robert C., et al. Microbial culturomics: paradigm shift in the human gut microbiome study. Clin. Microbiol. Infect. 2012; 18(12): 1185–93. https://doi.org/10.1111/1469-0691.12023
26. Maccaferri S., Biagi E., Brigidi P. Metagenomics: key to human gut microbiota. Dig. Dis. 2011; 29(6): 525–30. https://doi.org/10.1159/000332966
27. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA. 2010; 107(33): 14691–6. https://doi.org/10.1073/pnas.1005963107
28. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende Daniel R., et al. Enterotypes of the human gut microbiome. Nature. 2011; 473(7346): 174–80. https://doi.org/10.1038/nature09944
29. Biesbroek G., Tsivtsivadze E., Sanders E.A.M., Montijn R., Veenhoven R.H., Keijser B.J.F., et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am. J. Respir. Crit. Care Med. 2014; 190(11): 1283–92. https://doi.org/10.1164/rccm.201407-1240OC
30. Biesbroek G., Bosch A.A., Wang X., Keijser B.J., Veenhoven R.H., Sanders E.A., et al. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am. J. Respir. Crit. Care Med. 2014; 190(3): 298–308. https://doi.org/10.1164/rccm.201401-0073OC
31. Skowrońska A., Gawlik-Kotelnicka O., Margulska A., Strzelecki D. The influence of probiotic supplementation on the severity of anxiety and depressive symptoms; function and composition of gut microbiota; and metabolic, inflammation, and oxidative stress markers in patients with depression-a study protocol. Metabolites. 2023; 13(2): 182. https://doi.org/10.3390/metabo13020182
32. Schenck L.P., Surette M.G., Bowdish D.M. Composition and immunological significance of the upper respiratory tract microbiota. FEBS Lett. 2016; 590(21): 3705–20. https://doi.org/10.1002/1873-3468.12455
33. Bosch A.A.T.M., de Steenhuijsen Piters W.A.A., van Houten M.A., Chu M.L.J.N., Biesbroek G., Kool J., et al. Maturation of the infant respiratory microbiota, environmental drivers, and health consequences. a prospective cohort study. Am. J. Respir. Crit. Care Med. 2017; 196(12): 1582–90. https://doi.org/10.1164/rccm.201703-0554OC
34. Saito Y., Sagae T. Defecation status, intestinal microbiota, and habitual diet are associated with the fecal bile acid composition: a cross-sectional study in community-dwelling young participants. Eur. J. Nutr. 2023. https://doi.org/10.1007/s00394-023-03126-8
35. Kim C.H. Complex regulatory effects of gut microbial short-chain fatty acids on immune tolerance and autoimmunity. Cell. Mol. Immunol. 2023; 20(4): 341–50. https://doi.org/10.1038/s41423-023-00987-1
36. Alsharairi N.A. Therapeutic potential of gut microbiota and its metabolite short-chain fatty acids in neonatal necrotizing enterocolitis. Life (Basel). 2023; 13(2): 561. https://doi.org/10.3390/life13020561
37. Tokuno H., Itoga T., Kasuga J., Okuma K., Hasuko K., Masuyama H., et al. Method for estimating disease risk from microbiome data using structural equation modeling. Front. Microbiol. 2023; 14: 1035002. https://doi.org/10.3389/fmicb.2023.103500
Review
For citations:
Kurdyukova T.I., Krasnorutskaya O.N., Bugrimov D.Yu., Shevtsov A.N. Changes in the microbiota of the upper airways and intestine in the treatment of acute respiratory infections in preschool children. Russian Pediatric Journal. 2023;23(2):95-101. https://doi.org/10.46563/1560-9561-2023-26-2-95-101. EDN: sylbld