One strain of L. reuteri implies many options. Important issues in pediatrics
DOI: 10.32364/2618-8430-2022-5-1-72-77
S.V. Nikolaeva1, E.V. Kanner1, E.K. Shushakova1, A.A. Ploskireva1,2
1Central Research Institute of Epidemiology of the Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being, Moscow, Russian Federation
2Pirogov Russian National Research Medical University, Moscow, Russian Federation
Probiotics are living organisms that favor human health if administered in adequate amounts. In recent years, mechanisms of action of probiotics have been described. Moreover, strong evidence of their efficacy for preventing intestinal and respiratory infections, managing allergic and gastrointestinal disorders, and other pathologic conditions in children of different years was retrieved. Complex, physiological effects probiotics (if microbial strains are to be carefully selected and monitored for safety) contributed to the emergence of many probiotic preparations on the market. Lactobacillus reuteri, a well-known species of Lactobacillus, modulates immune response modulation, prevents infections and diseases, and is beneficial to human health. This paper addresses critical evidence of the efficacy of L. reuteri in children. Numerous clinical studies established its safety and tolerability. L. reuteri is effective for preventing and treating many diseases, including infantile colic, diarrhea, functional abdominal pain, atopic dermatitis, and allergy. L. reuteri is considered one of the available and effective medications for colic and other functional gastrointestinal disorders in children.
Keywords: children, probiotics, Lactobacillus reuteri, infantile colic, diarrhea, atopic dermatitis, allergy.
For citation: Nikolaeva S.V., Kanner E.V., Shushakova E.K., Ploskireva A.A. One strain of L. reuteri implies many options. Important issues in pediatrics. Russian Journal of Woman and Child Health. 2022;5(1):72–77 (in Russ.). DOI: 10.32364/2618-8430-2022-5-1-72-77.
Acknowledgements
The technical edition is supported by JSC "Alium".
Сведения об авторах:
Николаева Светлана Викторовна — к.м.н., старший научный сотрудник клинического отдела инфекционной патологии ФБУН ЦНИИ Эпидемиологии Роспотребнадзора; 111123, Россия, г. Москва, ул. Новогиреевская, д. 3А; ORCID iD 0000-0003-3880-8112.
Каннер Екатерина Валерьевна — д.м.н., старший научный сотрудник клинического отдела инфекционной патологии ФБУН ЦНИИ Эпидемиологии Роспотребнадзора; 111123, Россия, г. Москва, ул. Новогиреевская, д. 3А; ORCID iD 0000-0003-3204-1846.
Шушакова Екатерина Константиновна — младший научный сотрудник клинического отдела инфекционной патологии ФБУН ЦНИИ Эпидемиологии Роспотребнадзора; 111123, Россия, г. Москва, ул. Новогиреевская, д. 3А; ORCID iD 0000-0003-2619-9110.
Плоскирева Антонина Александровна — д.м.н., заместитель директора по клинической работе ФБУН ЦНИИ Эпидемиологии Роспотребнадзора; 111123, Россия, г. Москва, ул. Новогиреевская, д. 3А; профессор кафедры педиатрии с инфекционными болезнями у детей факультета дополнительного профессионального образования РНИМУ им. Н.И. Пирогова Минздрава России; 117997, Россия, г. Москва, ул. Островитянова, д. 1; ORCID iD 0000-0002-3612-1889.
Контактная информация: Николаева Светлана Викторовна, e-mail: nikolaeva008@list.ru.
Прозрачность финансовой деятельности: авторы не имеют финансовой заинтересованности в представленных материалах или методах.
Конфликт интересов отсутствует.
Статья поступила 03.11.2021.
Поступила после рецензирования 30.11.2021.
Принята в печать 23.12.2021.
About the authors:
Svetlana V. Nikolaeva — C. Sc. (Med.), senior researcher of the Clinical Division of Infectious Disorders, Central Research Institute of Epidemiology of the Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being; 3A, Novogireevskaya str., Moscow, 111123, Russian Federation; ORCID iD 0000-0003-3880-8112.
Ekaterina V. Kanner — Dr. Sc. (Med.), senior researcher of the Clinical Division of Infectious Disorders, Central Research Institute of Epidemiology of the Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being; 3A, Novogireevskaya str., Moscow, 111123, Russian Federation; ORCID iD 0000-0003-3204-1846.
Ekaterina K. Shushakova — junior researcher of the Clinical Division of Infectious Disorders, Central Research Institute of Epidemiology of the Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being; 3A, Novogireevskaya str., Moscow, 111123, Russian Federation; ORCID iD 0000-0003-2619-9110.
Antonina A. Ploskireva — Dr. Sc. (Med.), Deputy Director for Clinical Work, Central Research Institute of Epidemiology of the Russian Federal Service for Supervision of Consumer Rights Protection and Human Well-Being, 3A, Novogireevskaya str., Moscow, 111123, Russian Federation; professor of the Department of Pediatrics with Infectious Diseases in Children of the Faculty of Additional Professional Education, Pirogov Russian National Research Medical University; 1, Ostrovityanov str., Moscow, 117437, Russian Federation; ORCID iD 0000-0002-3612-1889.
Contact information: Svetlana V. Nikolaeva, e-mail: nikolaeva008@list.ru.
Financial Disclosure: no authors have a financial or property interest in any material or method mentioned.
There is no conflict of interests.
Received 03.11.2021.
Revised 30.11.2021.
Accepted 23.12.2021.
2. Bron P.A., van Baarlen P., Kleerebezem M. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat. Rev Genet. 2011;10:66–78. doi: 10.1038/nrmicro2690.
3. Mullish B.H., Marchesi J.R., McDonald J.A. et al. Probiotics reduce self-reported symptoms of upper respiratory tract infection in overweight and obese adults: Should we be considering probiotics during viral pandemics? Gut Microbes. 2021;13:1–9. doi: 10.1080/19490976.2021.1900997.
4. Lebeer S., Vanderleyden J., De Keersmaecker S.C. Host interactions of probiotic bacterial surface molecules: Comparison with commensals and pathogens. Nat Rev Genet. 2010;8:171–184. doi: 10.1038/nrmicro2297.
5. Cortes-Perez N.G., de Moreno de LeBlanc A., Gomez-Gutierrez J.G. et al. Probiotics and Trained Immunity. Biomolecules. 2021;11(10):1402. doi: 10.3390/biom11101402.
6. Fung T.C. The microbiota-immune axis as a central mediator of gut-brain communication. Neurobiol Dis. 2020;136:104714. doi:10.1016/j.nbd.2019.104714.
7. Belkaid Y., Harrison O.J. Homeostatic immunity and the microbiota. Immunity. 2017;46:562–576. DOI: 10.1016/j.immuni.2017.04.008.
8. О состоянии санитарно-эпидемиологического благополучия населения в Российской Федерации в 2020 году: Государственный доклад. М.: Федеральная служба по надзору в сфере защиты прав потребителей и благополучия человека; 2021. [On the state of sanitary and epidemiological well-being of the population in the Russian Federation in 2020: State report. Moscow: Federal Service for Supervision of Consumer Rights Protection and Human Welfare; 2021 (in Russ.)].
9. Cherian P.T., Wu X., Yang L. et al. Gastrointestinal localization of metronidazole by a lactobacilli-inspired tetramic acid motif improves treatment outcomes in the hamster model of Clostridium difficile infection. J Antimicrob Chemother. 2015;70:3061–3069. doi: 10.1093/jac/dkv231.
10. Abhisingha M., Dumnil J., Pitaksutheepong, C. Selection of Potential Probiotic Lactobacillus with Inhibitory Activity Against Salmonella and Fecal Coliform Bacteria. Probiotics Antimicrob Proteins. 2018;10:218–227. DOI: 10.1007/s12602-017-9304-8.
11. Genís S., Sánchez-Chardi A., Bach À. et al. A combination of lactic acid bacteria regulates Escherichia coli infection and inflammation of the bovine endometrium. J Dairy Sci. 2017;100(1):479–492. doi: 10.3168/jds.2016–11671.
12. Mukai T., Asasaka T., Sato E. et al. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol Med Microbiol. 2002;32(2):105–110. doi: 10.1111/j.1574–695X.2002.tb00541.x.
13. Lionetti E., Miniello V.L., Castellaneta S.P. et al. Lactobacillus reuteri therapy to reduce side-effects during anti-Helicobacter pylori treatment in children: a randomized placebo controlled trial. Aliment Pharmacol Ther. 2006;15;24(10):1461–1466. doi: 10.1111/j.1365–2036.2006.03145.x.
14. Ojetti V., Bruno G., Ainora M. E. et al. Impact of Lactobacillus reuteri supplementation on anti-Helicobacter pylori levofloxacin-based second-line therapy. Gastroenterol Res Pract. 2012:740381. doi: 10.1155/2012/740381.
15. Preidis G.A., Saulnier D.M., Blutt S.E. et al. Host response to probiotics determined by nutritional status of rotavirus-infected neonatal mice. J Pediatr Gastroenterol Nutr. 2012;55(3):299–307. doi: 10.1097/MPG.0b013e31824d2548.
16. Ang L.Y., Too H.K., Tan E.L. et al. Antiviral activity of Lactobacillus reuteri Protectis against Coxsackievirus A and Enterovirus 71 infection in human skeletal muscle and colon cell lines. Virol J. 2016;13:111. doi: 10.1186/s12985–016–0567–6.
17. Piyathilake C.J., Ollberding N.J., Kumar R. et al. Cervical Microbiota Associated with Higher Grade Cervical Intraepithelial Neoplasia in Women Infected with High-Risk Human Papillomaviruses. Cancer Prev Res (Phila). 2016;9(5):357–366. doi: 10.1158/1940–6207.CAPR-15–0350.
18. Jørgensen M.R., Kragelund C., Jensen P.Ø. et al. Probiotic Lactobacillus reuteri has antifungal effects on oral Candida species in vitro. J Oral Microbiol. 2017;9(1):1274582. doi: 10.1080/20002297.2016.1274582.
19. He B., Hoang T.K., Wang T. et al. Resetting microbiota by Lactobacillus reuteri inhibits T reg deficiency-induced autoimmunity via adenosine A2A receptors. J Exp Med. 2017;214(1):107–123. doi: 10.1084/jem.20160961.
20. Hsieh F.C., Lan C.C., Huang T.Y.. Heat-killed and live Lactobacillus reuteri GMNL-263 exhibit similar effects on improving metabolic functions in high-fat diet-induced obese rats. Food Funct. 2016;7(5):2374–2388. doi: 10.1039/c5fo01396h.
21. Lee J., Yang W., Hostetler A. et al. Characterization of the anti-inflammatory Lactobacillus reuteri BM36301 and its probiotic benefits on aged mice. BMC Microbiol. 2016;16:69. doi: 10.1186/s12866–016–0686–7.
22. Zelante T., Iannitti R.G., Cunha C. et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity. 2013;39(2):372–385. doi: 10.1016/j.immuni.2013.08.003.
23. Cervantes-Barragan L., Chai J.N., Tianero M.D. et al. Lactobacillus reuteri induces gut intraepithelial CD4+CD8αα+ T cells. Science. 2017;357(6353):806–810. doi: 10.1126/science.aah5825.
24. Nguyen N.T., Hanieh H., Nakahama T., Kishimoto T. The roles of aryl hydrocarbon receptor in immune responses. Int Immunol. 2013;25(6):335–343. doi: 10.1093/intimm/dxt011.
25. Mi G.L., Zhao L., Qiao D.D. et al. Effectiveness of Lactobacillus reuteri in infantile colic and colicky induced maternal depression: a prospective single blind randomized trial. Antonie Van Leeuwenhoek. 2015;107(6):1547–1543. doi: 10.1007/s10482–015–0448–9.
26. Savino F., Ceratto S., Poggi E. et al. Preventive effects of oral probiotic on infantile colic: a prospective, randomised, blinded, controlled trial using Lactobacillus reuteri DSM 17938. Benef Microbes. 2015;6(3):245–251. doi: 10.3920/BM2014.0090.
27. Gutierrez-Castrellon P., Lopez-Velazquez G., Diaz-Garcia L. et al. Diarrhea in preschool children and Lactobacillus reuteri: a randomized controlled trial. Pediatrics. 2014;133(4):e904–909. doi: 10.1542/peds.2013–0652.
28. Agustina R., Kok F.J., van de Rest O. et al. Randomized trial of probiotics and calcium on diarrhea and respiratory tract infections in Indonesian children. Pediatrics. 2012;129(5):e1155–1164. doi: 10.1542/peds.2011–1379.
29. Oncel M.Y., Sari F.N., Arayici S. et al. Lactobacillus Reuteri for the prevention of necrotising enterocolitis in very low birthweight infants: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2014;99(2):F110–115. doi: 10.1136/archdischild-2013–304745.
30. Abrahamsson T.R., Jakobsson T., Björkstén B. et al. No effect of probiotics on respiratory allergies: a seven-year follow-up of a randomized controlled trial in infancy. Pediatr Allergy Immunol. 2013;24(6):556–561. doi: 10.1111/pai.12104.
31. Rojas M.A., Lozano J.M., Rojas M.X. et al. Prophylactic probiotics to prevent death and nosocomial infection in preterm infants. Pediatrics. 2012;130(5):e1113–1120. doi: 10.1542/peds.2011–3584.
32. Rosenfeldt V., Benfeldt E., Nielsen S.D. et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol. 2003;111(2):389–395. doi: 10.1067/mai.2003.389.
33. Miniello V.L., Brunetti L., Tesse R. et al. Lactobacillus reuteri modulates cytokines production in exhaled breath condensate of children with atopic dermatitis. J Pediatr Gastroenterol Nutr. 2010;50(5):573–576. doi: 10.1097/MPG.0b013e3181bb343f.
34. Savino F., Pelle E., Palumeri E. et al. Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics. 2007;119(1):e124–130. doi: 10.1542/peds.2006–1222.
35. Savino F., Cresi F., Pautasso S. et al. Intestinal microflora in breastfed colicky and non-colicky infants. Acta Paediatr. 2004;93:825–829.
36. Savino F., Bailo E., Oggero R. et al. Bacterial counts of intestinal Lactobacillus species in infants with colic. Pediatr Allergy Immunol. 2005;16:72–75. DOI: 10.1111/j.1399-3038.2005.00207.x.
37. Savino F., Garro M., Montanari P. et al. Crying Time and RORγ/FOXP3 Expression in Lactobacillus reuteri DSM17938-Treated Infants with Colic: A Randomized Trial. J Pediatr. 2018;192:171–177.e1. doi: 10.1016/j.jpeds.2017.08.062.
38. Savino F., Cordisco L., Tarasco V. et al. Antagonistic effect of Lactobacillus strains against gas-producing coliforms isolated from colicky infants. BMC Microbiol. 2011;11:157. doi: 10.1186/1471–2180–11–157.
39. Pourmirzaiee M.A., Famouri F., Moazeni W., Hassanzadeh A. The efficacy of the prenatal administration of Lactobacillus reuteri LR92 DSM 26866 on the prevention of infantile colic: a randomized control trial. Eur J Pediatr. 2020;179(10):1619–1626. DOI: 10.1007/s00431-020-03641-4.
40. Mu Q., Tavella V.J., Luo X.M. Role of Lactobacillus reuteri in Human Health and Diseases. Front Microbiol. 2018;9:757. doi: 10.3389/fmicb.2018.00757.
41. Tanaka M., Nakayama J. Development of the gut microbiota in infancy and its impact on health in later life. Allergology International. 2017;66(4):515–522. DOI: 10.1016/j.alit.2017.07.010.
42. Sung V., D’Amico F., Cabana M.D. et al. Lactobacillus reuteri to Treat Infant Colic: A Meta-analysis. Pediatrics. 2018;141(1):e20171811. doi: 10.1542/peds.2017–1811.
43. Cruchet S., Furnes R., Maruy A. et al. The use of probiotics in pediatric gastroenterology: a review of the literature and recommendations by Latin-American experts. Paediatr Drugs. 2015;17(3):199–216. doi: 10.1007/s40272–015–0124–6.
This work is licensed under a Creative Commons «Attribution» 4.0 License.
