Single-Strain Probiotic Lactobacilli for the Treatment of Atopic Dermatitis in Children: A Systematic Review and Meta-Analysis

Sabina Fijan, Nina Kolč, Metka Hrašovec, Gro Jamtvedt, Maja Šikić Pogačar, Dušanka Mičetić Turk, Uroš Maver, Sabina Fijan, Nina Kolč, Metka Hrašovec, Gro Jamtvedt, Maja Šikić Pogačar, Dušanka Mičetić Turk, Uroš Maver

Abstract

Probiotics are known for their positive effects on the gut microbiota. There is growing evidence that the infant gut and skin colonization have a role in the development of the immune system, which may be helpful in the prevention and treatment of atopic dermatitis. This systematic review focused on evaluating the effect of single-strain probiotic lactobacilli consumption on treating children's atopic dermatitis. Seventeen randomized placebo-controlled trials with the primary outcome of the Scoring Atopic Dermatitis (SCORAD) index were included in the systematic review. Clinical trials using single-strain lactobacilli were included. The search was conducted until October 2022 using PubMed, ScienceDirect, Web of Science, Cochrane library and manual searches. The Joanna Briggs Institute appraisal tool was used to assess the quality of the included studies. Meta-analyses and sub meta-analyses were performed using Cochrane Collaboration methodology. Due to different methods of reporting the SCORAD index, only 14 clinical trials with 1124 children were included in the meta-analysis (574 in the single-strain probiotic lactobacilli group and 550 in the placebo group) and showed that single-strain probiotic lactobacilli statistically significantly reduced the SCORAD index compared to the placebo in children with atopic dermatitis (mean difference [MD]: -4.50; 95% confidence interval [CI]: -7.50 to -1.49; Z = 2.93; p = 0.003; heterogeneity I2 = 90%). The subgroup meta-analysis showed that strains of Limosilactobacillus fermentum were significantly more effective than strains of Lactiplantibacillus plantarum, Lacticaseibacillus paracasei or Lacticaseibacillus rhamnosus. A longer treatment time and younger treatment age statistically significantly reduced symptoms of atopic dermatitis. The result of this systematic review and meta-analysis shows that certain single-strain probiotic lactobacilli are more successful than others in reducing atopic dermatitis severity in children. Therefore, careful consideration to strain selection, treatment time and the age of the treated patients are important factors in enhancing the effectiveness of reducing atopic dermatitis in children when choosing probiotic single-strain lactobacilli.

Keywords: atopic dermatitis; children; lactobacilli; meta-analysis; probiotics; systematic review.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
PRISMA flow chart of the study selection process.
Figure 2
Figure 2
Meta-analysis of the effect of single-strain probiotic lactobacilli compared to placebo on the SCORAD index change in children with AD [41,42,43,44,46,47,48,49,50,51,52,53,54,55].
Figure 3
Figure 3
Subgroup meta-analyses of the effect of the included single-strain probiotic Lacticaseibacillus rhamnosus, Limosilactobacillus fermentum, Lacticaseibacillus paracasei and Lactiplantibacillus plantarum strains compared to placebo on the SCORAD index change in children with AD [41,42,43,44,46,47,49,50,51,52,53,54].
Figure 3
Figure 3
Subgroup meta-analyses of the effect of the included single-strain probiotic Lacticaseibacillus rhamnosus, Limosilactobacillus fermentum, Lacticaseibacillus paracasei and Lactiplantibacillus plantarum strains compared to placebo on the SCORAD index change in children with AD [41,42,43,44,46,47,49,50,51,52,53,54].
Figure 4
Figure 4
Subgroup meta-analyses of the effect of 8 weeks treatment time with single-strain probiotic lactobacilli compared to placebo on the SCORAD index change in children with AD [41,44,46,54].
Figure 5
Figure 5
Subgroup meta-analyses of the effect of 12 weeks treatment time with single-strain probiotic lactobacilli compared to placebo on the SCORAD index change in children with AD [42,48,49,50,51,52,53,54,55].
Figure 6
Figure 6
Subgroup meta-analyses of the effect of single-strain probiotic lactobacilli compared to placebo on the SCORAD index change in children with moderate to severe AD [44,46,49].
Figure 7
Figure 7
Subgroup meta-analyses of the effect of single-strain probiotic lactobacilli compared to placebo on the SCORAD index change without studies of children with moderate to severe AD [41,42,43,47,48,50,51,52,53,54,55].
Figure 8
Figure 8
Subgroup meta-analyses of the effect of single-strain probiotic lactobacilli compared to placebo on the SCORAD index change in children up to 4 years of age [41,42,43,44,47,49,50,54,55].
Figure 9
Figure 9
Subgroup meta-analyses of the effect of 3 months supplementation with Lacticaseibacillus rhamnosus GG (LGG) compared to placebo on the SCORAD index change in children with AD aged under 1 year at treatment time [41,42].

References

    1. Powers C.E., McShane D.B., Gilligan P.H., Burkhart C.N., Morrell D.S. Microbiome and pediatric atopic dermatitis. J. Dermatol. 2015;42:1137–1142. doi: 10.1111/1346-8138.13072.
    1. Williams H.C., Burden-Teh E. On the definition of dermatological disease. Part 2: Approaches for defining dermatological diseases. Clin. Exp. Dermatol. 2022;47:1812–1819. doi: 10.1111/ced.15278.
    1. Raimondo A., Lembo S. Atopic Dermatitis: Epidemiology and Clinical Phenotypes. Dermatol. Pract. Concept. 2021;11:e2021146. doi: 10.5826/dpc.1104a146.
    1. Johnson H., Yu J. Current and Emerging Therapies in Pediatric Atopic Dermatitis. Dermatol. Ther. 2022;12:2691–2703. doi: 10.1007/s13555-022-00829-4.
    1. Oranje A.P. Practical issues on interpretation of scoring atopic dermatitis: SCORAD Index, objective SCORAD, patient-oriented SCORAD and Three-Item Severity score. Curr. Probl. Dermatol. 2011;41:149–155. doi: 10.1159/000323308.
    1. Chopra R., Vakharia P.P., Sacotte R., Patel N., Immaneni S., White T., Kantor R., Hsu D.Y., Silverberg J.I. Severity strata for Eczema Area and Severity Index (EASI), modified EASI, Scoring Atopic Dermatitis (SCORAD), objective SCORAD, Atopic Dermatitis Severity Index and body surface area in adolescents and adults with atopic dermatitis. Br. J. Dermatol. 2017;177:1316–1321. doi: 10.1111/bjd.15641.
    1. Oranje A.P., Glazenburg E.J., Wolkerstorfer A., de Waard-van der Spek F.B. Practical issues on interpretation of scoring atopic dermatitis: The SCORAD index, objective SCORAD and the three-item severity score. Br. J. Dermatol. 2007;157:645–648. doi: 10.1111/j.1365-2133.2007.08112.x.
    1. Shi B., Bangayan N.J., Curd E., Taylor P.A., Gallo R.L., Leung D.Y.M., Li H. The skin microbiome is different in pediatric versus adult atopic dermatitis. J. Allergy Clin. Immunol. 2016;138:1233–1236. doi: 10.1016/j.jaci.2016.04.053.
    1. Gupta M., Sicherer S.H. Timing of food introduction and atopy prevention. Clin. Dermatol. 2017;35:398–405. doi: 10.1016/j.clindermatol.2017.03.013.
    1. Arkwright P.D., Koplin J.J. Impact of a Decade of Research into Atopic Dermatitis. J. Allergy Clin. Immunol. Pract. 2022;11:63–71. doi: 10.1016/j.jaip.2022.09.021.
    1. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S., et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Zheng J., Wittouck S., Salvetti E., Franz C., Harris H.M.B., Mattarelli P., O’Toole P.W., Pot B., Vandamme P., Walter J., et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 2020;70:2782–2858. doi: 10.1099/ijsem.0.004107.
    1. Fijan S. Microorganisms with Claimed Probiotic Properties: An Overview of Recent Literature. Int. J. Environ. Res. Public Health. 2014;11:4745–4767. doi: 10.3390/ijerph110504745.
    1. Fuchs-Tarlovsky V., Marquez-Barba M.F., Sriram K. Probiotics in dermatologic practice. Nutrition. 2016;32:289–295. doi: 10.1016/j.nut.2015.09.001.
    1. Ganji-Arjenaki M., Rafieian-Kopaei M. Probiotics are a good choice in remission of inflammatory bowel diseases: A meta analysis and systematic review. J. Cell Physiol. 2018;233:2091–2103. doi: 10.1002/jcp.25911.
    1. Holte K., Krag A., Gluud L.L. Systematic review and meta-analysis of randomized trials on probiotics for hepatic encephalopathy. Hepatol Res. 2012;42:1008–1015. doi: 10.1111/j.1872-034X.2012.01015.x.
    1. Hungin A.P., Mulligan C., Pot B., Whorwell P., Agréus L., Fracasso P., Lionis C., Mendive J., Philippart de Foy J.M., Rubin G., et al. Systematic review: Probiotics in the management of lower gastrointestinal symptoms in clinical practice—An evidence-based international guide. Aliment Pharmacol. Ther. 2013;38:864–886. doi: 10.1111/apt.12460.
    1. Salem I., Ramser A., Isham N., Ghannoum M.A. The Gut Microbiome as a Major Regulator of the Gut-Skin Axis. Front. Microbiol. 2018;9:1459. doi: 10.3389/fmicb.2018.01459.
    1. Clarke G., Stilling R.M., Kennedy P.J., Stanton C., Cryan J.F., Dinan T.G. Minireview: Gut Microbiota: The Neglected Endocrine Organ. Mol. Endocrinol. 2014;28:1221–1238. doi: 10.1210/me.2014-1108.
    1. Maldonado Galdeano C., Cazorla S.I., Lemme Dumit J.M., Vélez E., Perdigón G. Beneficial Effects of Probiotic Consumption on the Immune System. Ann. Nutr. Metab. 2019;74:115–124. doi: 10.1159/000496426.
    1. Liu Y., Alookaran J.J., Rhoads J.M. Probiotics in Autoimmune and Inflammatory Disorders. Nutrients. 2018;10:1537. doi: 10.3390/nu10101537.
    1. Kerry R.G., Patra J.K., Gouda S., Park Y., Shin H.S., Das G. Benefaction of probiotics for human health: A review. J. Food Drug Anal. 2018;26:927–939. doi: 10.1016/j.jfda.2018.01.002.
    1. Zhu G., Zhao J., Zhang H., Chen W., Wang G. Probiotics for Mild Cognitive Impairment and Alzheimer’s Disease: A Systematic Review and Meta-Analysis. Foods. 2021;10:1672. doi: 10.3390/foods10071672.
    1. Binda S., Hill C., Johansen E., Obis D., Pot B., Sanders M.E., Tremblay A., Ouwehand A.C. Criteria to Qualify Microorganisms as "Probiotic" in Foods and Dietary Supplements. Front. Microbiol. 2020;11:1662. doi: 10.3389/fmicb.2020.01662.
    1. Rautava S., Kalliomäki M., Isolauri E. New therapeutic strategy for combating the increasing burden of allergic disease: Probiotics-A Nutrition, Allergy, Mucosal Immunology and Intestinal Microbiota (NAMI) Research Group report. J. Allergy Clin. Immunol. 2005;116:31–37. doi: 10.1016/j.jaci.2005.02.010.
    1. Anania C., Brindisi G., Martinelli I., Bonucci E., D’Orsi M., Ialongo S., Nyffenegger A., Raso T., Spatuzzo M., De Castro G., et al. Probiotics Function in Preventing Atopic Dermatitis in Children. Int. J. Mol. Sci. 2022;23:5409. doi: 10.3390/ijms23105409.
    1. Liu Y., Du X., Zhai S., Tang X., Liu C., Li W. Gut microbiota and atopic dermatitis in children: A scoping review. BMC Pediatr. 2022;22:323. doi: 10.1186/s12887-022-03390-3.
    1. Boggio Marzet C., Burgos F., Del Compare M., Gerold I., Tabacco O., Vinderola G. Approach to probiotics in pediatrics: The role of Lactobacillus rhamnosus GG. Arch. Argent Pediatr. 2022;120:e1–e7. doi: 10.5546/aap.2022.eng.e1.
    1. Jiang W., Ni B., Liu Z., Liu X., Xie W., Wu I.X.Y., Li X. The Role of Probiotics in the Prevention and Treatment of Atopic Dermatitis in Children: An Updated Systematic Review and Meta-Analysis of Randomized Controlled Trials. Paediatr. Drugs. 2020;22:535–549. doi: 10.1007/s40272-020-00410-6.
    1. Sun S., Chang G., Zhang L. The prevention effect of probiotics against eczema in children: An update systematic review and meta-analysis. J. Dermatol. Treat. 2022;33:1844–1854. doi: 10.1080/09546634.2021.1925077.
    1. D’Elios S., Trambusti I., Verduci E., Ferrante G., Rosati S., Marseglia G.L., Drago L., Peroni D.G. Probiotics in the prevention and treatment of atopic dermatitis. Pediatr. Allergy Immunol. 2020;31((Suppl. 26)):43–45. doi: 10.1111/pai.13364.
    1. Huang R., Ning H., Shen M., Li J., Zhang J., Chen X. Probiotics for the Treatment of Atopic Dermatitis in Children: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Front. Cell Infect. Microbiol. 2017;7:392. doi: 10.3389/fcimb.2017.00392.
    1. Higgins J.P.T., López-López J.A., Becker B.J., Davies S.R., Dawson S., Grimshaw J.M., McGuinness L.A., Moore T.H.M., Rehfuess E.A., Thomas J., et al. Synthesising quantitative evidence in systematic reviews of complex health interventions. BMJ Glob. Health. 2019;4:e000858. doi: 10.1136/bmjgh-2018-000858.
    1. Page M.J., McKenzie J.E., Bossuyt P.M., Boutron I., Hoffmann T.C., Mulrow C.D., Shamseer L., Tetzlaff J.M., Akl E.A., Brennan S.E., et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. PLoS Med. 2021;18:e1003583. doi: 10.1371/journal.pmed.1003583.
    1. Tufanaru C., Munn Z., Aromataris E., Campbell J., Hopp L. Chapter 3: Systematic reviews of effectiveness. In: Aromataris E., Munn Z., editors. JBI Manual for Evidence Synthesis. JBI, University of Adelaide; Adelaide, Australia: 2020.
    1. Camp S., Legge T. Simulation as a Tool for Clinical Remediation: An Integrative Review. Clin. Simul. Nurs. 2018;16:48–61. doi: 10.1016/j.ecns.2017.11.003.
    1. Higgins J.P., Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.2.0. 2017. [(accessed on 3 November 2022)]. Available online: .
    1. Cumpston M.S., McKenzie J.E., Welch V.A., Brennan S.E. Strengthening systematic reviews in public health: Guidance in the Cochrane Handbook for Systematic Reviews of Interventions, 2nd edition. J. Public Health. 2022;44:e588–e592. doi: 10.1093/pubmed/fdac036.
    1. Luo D., Wan X., Liu J., Tong T. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat. Methods Med. Res. 2018;27:1785–1805. doi: 10.1177/0962280216669183.
    1. Wan X., Wang W., Liu J., Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med. Res. Methodol. 2014;14:135. doi: 10.1186/1471-2288-14-135.
    1. Isolauri E., Arvola T., Sütas Y., Moilanen E., Salminen S. Probiotics in the management of atopic eczema. Clin. Exp. Allergy. 2000;30:1604–1610. doi: 10.1046/j.1365-2222.2000.00943.x.
    1. Kirjavainen P.V., Salminen S.J., Isolauri E. Probiotic bacteria in the management of atopic disease: Underscoring the importance of viability. J. Pediatr. Gastroenterol. Nutr. 2003;36:223–227. doi: 10.1097/00005176-200302000-00012.
    1. Viljanen M., Savilahti E., Haahtela T., Juntunen-Backman K., Korpela R., Poussa T., Tuure T., Kuitunen M. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: A double-blind placebo-controlled trial. Allergy. 2005;60:494–500. doi: 10.1111/j.1398-9995.2004.00514.x.
    1. Weston S., Halbert A., Richmond P., Prescott S.L. Effects of probiotics on atopic dermatitis: A randomised controlled trial. Arch. Dis. Child. 2005;90:892–897. doi: 10.1136/adc.2004.060673.
    1. Brouwer M.L., Wolt-Plompen S.A., Dubois A.E., van der Heide S., Jansen D.F., Hoijer M.A., Kauffman H.F., Duiverman E.J. No effects of probiotics on atopic dermatitis in infancy: A randomized placebo-controlled trial. Clin. Exp. Allergy. 2006;36:899–906. doi: 10.1111/j.1365-2222.2006.02513.x.
    1. Fölster-Holst R., Müller F., Schnopp N., Abeck D., Kreiselmaier I., Lenz T., von Rüden U., Schrezenmeir J., Christophers E., Weichenthal M. Prospective, randomized controlled trial on Lactobacillus rhamnosus in infants with moderate to severe atopic dermatitis. Br. J. Dermatol. 2006;155:1256–1261. doi: 10.1111/j.1365-2133.2006.07558.x.
    1. Grüber C., Wendt M., Sulser C., Lau S., Kulig M., Wahn U., Werfel T., Niggemann B. Randomized, placebo-controlled trial of Lactobacillus rhamnosus GG as treatment of atopic dermatitis in infancy. Allergy. 2007;62:1270–1276. doi: 10.1111/j.1398-9995.2007.01543.x.
    1. Woo S.I., Kim J.Y., Lee Y.J., Kim N.S., Hahn Y.S. Effect of Lactobacillus sakei supplementation in children with atopic eczema-dermatitis syndrome. Ann. Allergy Asthma Immunol. 2010;104:343–348. doi: 10.1016/j.anai.2010.01.020.
    1. Klewicka E., Cukrowska B., Libudzisz Z., Slizewska K., Motyl I. Changes in gut microbiota in children with atopic dermatitis administered the bacteria Lactobacillus casei DN--114001. Pol. J. Microbiol. 2011;60:329–333. doi: 10.33073/pjm-2011-047.
    1. Gore C., Custovic A., Tannock G.W., Munro K., Kerry G., Johnson K., Peterson C., Morris J., Chaloner C., Murray C.S., et al. Treatment and secondary prevention effects of the probiotics Lactobacillus paracasei or Bifidobacterium lactis on early infant eczema: Randomized controlled trial with follow-up until age 3 years. Clin. Exp. Allergy. 2012;42:112–122. doi: 10.1111/j.1365-2222.2011.03885.x.
    1. Han Y., Kim B., Ban J., Lee J., Kim B.J., Choi B.S., Hwang S., Ahn K., Kim J. A randomized trial of Lactobacillus plantarum CJLP133 for the treatment of atopic dermatitis. Pediatr. Allergy Immunol. 2012;23:667–673. doi: 10.1111/pai.12010.
    1. Wang I.J., Wang J.Y. Children with atopic dermatitis show clinical improvement after Lactobacillus exposure. Clin. Exp. Allergy. 2015;45:779–787. doi: 10.1111/cea.12489.
    1. Prakoeswa C.R.S., Herwanto N., Prameswari R., Astari L., Sawitri S., Hidayati A.N., Indramaya D.M., Kusumowidagdo E.R., Surono I.S. Lactobacillus plantarum IS-10506 supplementation reduced SCORAD in children with atopic dermatitis. Benef. Microbes. 2017;8:833–840. doi: 10.3920/BM2017.0011.
    1. Wu Y.J., Wu W.F., Hung C.W., Ku M.S., Liao P.F., Sun H.L., Lu K.H., Sheu J.N., Lue K.H. Evaluation of efficacy and safety of Lactobacillus rhamnosus in children aged 4-48 months with atopic dermatitis: An 8-week, double-blind, randomized, placebo-controlled study. J. Microbiol. Immunol. Infect. 2017;50:684–692. doi: 10.1016/j.jmii.2015.10.003.
    1. Ahn S.H., Yoon W., Lee S.Y., Shin H.S., Lim M.Y., Nam Y.D., Yoo Y. Effects of Lactobacillus pentosus in Children with Allergen-Sensitized Atopic Dermatitis. J. Korean Med. Sci. 2020;35:e128. doi: 10.3346/jkms.2020.35.e128.
    1. Rather I.A., Kim B.C., Lew L.C., Cha S.K., Lee J.H., Nam G.J., Majumder R., Lim J., Lim S.K., Seo Y.J., et al. Oral Administration of Live and Dead Cells of Lactobacillus sakei proBio65 Alleviated Atopic Dermatitis in Children and Adolescents: A Randomized, Double-Blind, and Placebo-Controlled Study. Probiotics Antimicrob. Proteins. 2021;13:315–326. doi: 10.1007/s12602-020-09654-7.
    1. Carucci L., Nocerino R., Paparo L., De Filippis F., Coppola S., Giglio V., Cozzolino T., Valentino V., Sequino G., Bedogni G., et al. Therapeutic effects elicited by the probiotic Lacticaseibacillus rhamnosus GG in children with atopic dermatitis. The results of the ProPAD trial. Pediatr. Allergy Immunol. 2022;33:e13836. doi: 10.1111/pai.13836.
    1. Kim S.-O., Ah Y.-M., Yu Y.M., Choi K.H., Shin W.-G., Lee J.-Y. Effects of probiotics for the treatment of atopic dermatitis: A meta-analysis of randomized controlled trials. Ann. Allergy Asthma Immunol. 2014;113:217–226. doi: 10.1016/j.anai.2014.05.021.
    1. Pessi T., Sütas Y., Hurme M., Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin. Exp. Allergy. 2000;30:1804–1808. doi: 10.1046/j.1365-2222.2000.00948.x.
    1. Steiner N.C., Lorentz A. Probiotic Potential of Lactobacillus Species in Allergic Rhinitis. Int. Arch. Allergy Immunol. 2021;182:807–818. doi: 10.1159/000515352.
    1. Bianchini S., Orabona C., Camilloni B., Berioli M.G., Argentiero A., Matino D., Alunno A., Albini E., Vacca C., Pallotta M.T., et al. Effects of probiotic administration on immune responses of children and adolescents with type 1 diabetes to a quadrivalent inactivated influenza vaccine. Hum. Vaccines Immunother. 2020;16:86–94. doi: 10.1080/21645515.2019.1633877.
    1. Naghmouchi K., Belguesmia Y., Bendali F., Spano G., Seal B.S., Drider D. Lactobacillus fermentum: A bacterial species with potential for food preservation and biomedical applications. Crit. Rev. Food Sci. Nutr. 2020;60:3387–3399. doi: 10.1080/10408398.2019.1688250.
    1. Gupta T., Kaur H., Kapila S., Kapila R. Lactobacillus fermentum (MTCC-5898) alleviates Escherichia coli-induced inflammatory responses in intestinal epithelial cells by modulating immune genes and NF-κB signalling. J. Appl. Microbiol. 2021;131:3008–3017. doi: 10.1111/jam.15153.
    1. Lee C.S., Kim S.H. Anti-inflammatory and Anti-osteoporotic Potential of Lactobacillus plantarum A41 and L. fermentum SRK414 as Probiotics. Probiotics Antimicrob. Proteins. 2020;12:623–634. doi: 10.1007/s12602-019-09577-y.
    1. Viljanen M., Kuitunen M., Haahtela T., Juntunen-Backman K., Korpela R., Savilahti E. Probiotic effects on faecal inflammatory markers and on faecal IgA in food allergic atopic eczema/dermatitis syndrome infants. Pediatr. Allergy Immunol. 2005;16:65–71. doi: 10.1111/j.1399-3038.2005.00224.x.
    1. Viljanen M., Pohjavuori E., Haahtela T., Korpela R., Kuitunen M., Sarnesto A., Vaarala O., Savilahti E. Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome. J. Allergy Clin. Immunol. 2005;115:1254–1259. doi: 10.1016/j.jaci.2005.03.047.
    1. Wickens K., Black P.N., Stanley T.V., Mitchell E., Fitzharris P., Tannock G.W., Purdie G., Crane J. A differential effect of 2 probiotics in the prevention of eczema and atopy: A double-blind, randomized, placebo-controlled trial. J. Allergy Clin. Immunol. 2008;122:788–794. doi: 10.1016/j.jaci.2008.07.011.
    1. Simpson M.R., Dotterud C.K., Storrø O., Johnsen R., Øien T. Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial. BMC Dermatol. 2015;15:13. doi: 10.1186/s12895-015-0030-1.
    1. Wickens K., Black P., Stanley T.V., Mitchell E., Barthow C., Fitzharris P., Purdie G., Crane J. A protective effect of Lactobacillus rhamnosus HN001 against eczema in the first 2 years of life persists to age 4 years. Clin. Exp. Allergy. 2012;42:1071–1079. doi: 10.1111/j.1365-2222.2012.03975.x.
    1. Rose M.A., Stieglitz F., Köksal A., Schubert R., Schulze J., Zielen S. Efficacy of probiotic Lactobacillus GG on allergic sensitization and asthma in infants at risk. Clin. Exp. Allergy. 2010;40:1398–1405. doi: 10.1111/j.1365-2222.2010.03560.x.
    1. Moro G., Arslanoglu S., Stahl B., Jelinek J., Wahn U., Boehm G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch. Dis. Child. 2006;91:814–819. doi: 10.1136/adc.2006.098251.
    1. Shafiei A., Moin M., Pourpak Z., Gharagozlou M., Aghamohamadi A., Sajedi V., Soheili H., Sotoodeh S., Movahedi M. Synbiotics could not Reduce the Scoring of Childhood Atopic Dermatitis (SCORAD): A Randomized Double Blind Placebo-Controlled Trial. Iran. J. Allergy Asthma Immunol. 2011;10:21–28.
    1. Sharma R., Honda S., Mahajan R., De D., Sachdeva N. Evaluating the Effect of Supplementation with Bacillus clausii on Therapeutic Outcomes in Atopic Eczema-Results of an Observer-Blinded Parallel-Group Randomized Controlled Study. Indian J. Dermatol. 2022;67:121–126. doi: 10.4103/ijd.ijd_587_21.
    1. Ivakhnenko E.S., Nian’kovskiĭ S.L. Effect of probiotics on the dynamics of gastrointestinal symptoms of food allergy to cow’s milk protein in infants. Georgian Med. News. 2013;219:46–52.
    1. van der Aa L.B., Lutter R., Heymans H.S., Smids B.S., Dekker T., van Aalderen W.M., Sillevis Smitt J.H., Knippels L.M., Garssen J., Nauta A.J., et al. No detectable beneficial systemic immunomodulatory effects of a specific synbiotic mixture in infants with atopic dermatitis. Clin. Exp. Allergy. 2012;42:531–539. doi: 10.1111/j.1365-2222.2011.03890.x.
    1. Navarro-Lopez V., Ramirez-Bosca A., Ramon-Vidal D., Ruzafa-Costas B., Genoves-Martinez S., Chenoll-Cuadros E., Carrion-Gutierrez M., de la Parte J.H., Prieto-Merino D., Codoner-Cortes F.M. Effect of Oral Administration of a Mixture of Probiotic Strains on SCORAD Index and Use of Topical Steroids in Young Patients With Moderate Atopic Dermatitis A Randomized Clinical Trial. JAMA Dermatol. 2018;154:37–43. doi: 10.1001/jamadermatol.2017.3647.
    1. Kim J.Y., Kwon J.H., Ahn S.H., Lee S.I., Han Y.S., Choi Y.O., Lee S.Y., Ahn K.M., Ji G.E. Effect of probiotic mix (Bifidobacterium bifidum, Bifidobacterium lactis, Lactobacillus acidophilus) in the primary prevention of eczema: A double-blind, randomized, placebo-controlled trial. Pediatr. Allergy Immunol. 2010;21:e386–e393. doi: 10.1111/j.1399-3038.2009.00958.x.
    1. Gerasimov S.V., Vasjuta V.V., Myhovych O.O., Bondarchuk L.I. Probiotic supplement reduces atopic dermatitis in preschool children: A randomized, double-blind, placebo-controlled, clinical trial. Am. J. Clin. Dermatol. 2010;11:351–361. doi: 10.2165/11531420-000000000-00000.
    1. Rosenfeldt V., Benfeldt E., Nielsen S.D., Michaelsen K.F., Jeppesen D.L., Valerius N.H., Paerregaard A. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J. Allergy Clin. Immunol. 2003;111:389–395. doi: 10.1067/mai.2003.389.
    1. Cukrowska B., Ceregra A., Maciorkowska E., Surowska B., Zegadło-Mylik M.A., Konopka E., Trojanowska I., Zakrzewska M., Bierła J.B., Zakrzewski M., et al. The Effectiveness of Probiotic Lactobacillus rhamnosus and Lactobacillus casei Strains in Children with Atopic Dermatitis and Cow’s Milk Protein Allergy: A Multicenter, Randomized, Double Blind, Placebo Controlled Study. Nutrients. 2021;13:1169. doi: 10.3390/nu13041169.
    1. Farid R., Ahanchian H., Jabbari F., Moghiman T. Effect of a New Synbiotic Mixture on Atopic Dermatitis in Children: A Randomized-Controlled Trial. Iran. J. Pediatr. 2011;21:225–230.
    1. D’Auria E., Panelli S., Lunardon L., Pajoro M., Paradiso L., Beretta S., Loretelli C., Tosi D., Perini M., Bedogni G., et al. Rice flour fermented with Lactobacillus paracasei CBA L74 in the treatment of atopic dermatitis in infants: A randomized, double- blind, placebo- controlled trial. Pharmacol. Res. 2021;163:105284. doi: 10.1016/j.phrs.2020.105284.
    1. Jeong K., Kim M., Jeon S.A., Kim Y.H., Lee S. A randomized trial of Lactobacillus rhamnosus IDCC 3201 tyndallizate (RHT3201) for treating atopic dermatitis. Pediatr. Allergy Immunol. 2020;31:783–792. doi: 10.1111/pai.13269.
    1. Nakata J., Hirota T., Umemura H., Nakagawa T., Kando N., Futamura M., Nakamura Y., Ito K. Additive effect of Lactobacillus acidophilus L-92 on children with atopic dermatitis concomitant with food allergy. Asia Pac. Allergy. 2019;9:e18. doi: 10.5415/apallergy.2019.9.e18.
    1. Yan D.C., Hung C.H., Sy L.B., Lue K.H., Shih I.H., Yang C.Y., Chen L.C., Sun H.L., Lee M.S., Chambard J., et al. A Randomized, Double-Blind, Placebo-Controlled Trial Assessing the Oral Administration of a Heat-Treated Lactobacillus paracasei Supplement in Infants with Atopic Dermatitis Receiving Topical Corticosteroid Therapy. Skin Pharmacol. Physiol. 2019;32:201–211. doi: 10.1159/000499436.
    1. Passeron T., Lacour J.P., Fontas E., Ortonne J.P. Prebiotics and synbiotics: Two promising approaches for the treatment of atopic dermatitis in children above 2 years. Allergy. 2006;61:431–437. doi: 10.1111/j.1398-9995.2005.00956.x.
    1. Aldaghi M., Tehrani H., Karrabi M., Abadi F.S., Sahebkar M. The effect of multi-strain synbiotic and vitamin D3 supplements on the severity of atopic dermatitis among infants under 1 year of age: A double-blind, randomized clinical trial study. J. Dermatol. Treat. 2022;33:812–817. doi: 10.1080/09546634.2020.1782319.
    1. Rozé J.C., Barbarot S., Butel M.J., Kapel N., Waligora-Dupriet A.J., De Montgolfier I., Leblanc M., Godon N., Soulaines P., Darmaun D., et al. An α-lactalbumin-enriched and symbiotic-supplemented v. a standard infant formula: A multicentre, double-blind, randomised trial. Br. J. Nutr. 2012;107:1616–1622. doi: 10.1017/S000711451100479X.
    1. Wu K.G., Li T.H., Peng H.J. Lactobacillus salivarius plus fructo-oligosaccharide is superior to fructo-oligosaccharide alone for treating children with moderate to severe atopic dermatitis: A double-blind, randomized, clinical trial of efficacy and safety. Br. J. Dermatol. 2012;166:129–136. doi: 10.1111/j.1365-2133.2011.10596.x.
    1. Zhao M., Shen C., Ma L. Treatment efficacy of probiotics on atopic dermatitis, zooming in on infants: A systematic review and meta-analysis. Int. J. Dermatol. 2018;57:635–641. doi: 10.1111/ijd.13873.
    1. Lambring C.B., Siraj S., Patel K., Sankpal U.T., Mathew S., Basha R. Impact of the Microbiome on the Immune System. Crit. Rev. Immunol. 2019;39:313–328. doi: 10.1615/CritRevImmunol.2019033233.
    1. Eslami M., Bahar A., Keikha M., Karbalaei M., Kobyliak N.M., Yousefi B. Probiotics function and modulation of the immune system in allergic diseases. Allergol. Immunopathol. 2020;48:771–788. doi: 10.1016/j.aller.2020.04.005.
    1. Fenner J., Silverberg N.B. Oral supplements in atopic dermatitis. Clin. Dermatol. 2018;36:653–658. doi: 10.1016/j.clindermatol.2018.05.010.
    1. Boulos S., Yan A.C. Current concepts in the prevention of atopic dermatitis. Clin. Dermatol. 2018;36:668–671. doi: 10.1016/j.clindermatol.2017.03.004.
    1. Elghazaly S.M., Hamam K.M., Badawy M.M., Yakoub Agha N.A., Samy A., Abbas A.M. Efficacy and safety of single dose of oral secnidazole 2 g in treatment of bacterial vaginosis: A systematic review and meta-analysis. Eur. J. Obstet Gynecol. Reprod. Biol. 2019;238:125–131. doi: 10.1016/j.ejogrb.2019.05.013.
    1. Yao Z., Chen H., Wang X., Zhang Y., Jian M., Hu J., Yu B., Jiang L. Efficacy of the Short-Term versus Long-Term Administration of Antimicrobial Prophylaxis in Gastric Cancer Surgery: A Meta-Analysis of Randomized Controlled Trials. Surg. Infect. 2022;23:625–633. doi: 10.1089/sur.2022.179.
    1. Janjua S., Mathioudakis A.G., Fortescue R., Walker R.A.E., Sharif S., Threapleton C.J.D., Dias S. Prophylactic antibiotics for adults with chronic obstructive pulmonary disease: A network meta-analysis. Cochrane Database Syst. Rev. 2021;1:CD013198. doi: 10.1002/14651858.CD013198.
    1. Ricci G., Cipriani F., Cuello-Garcia C.A., Brożek J.L., Fiocchi A., Pawankar R., Yepes-Nuñes J.J., Terraciano L., Gandhi S., Agarwal A., et al. A clinical reading on “World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics”. World Allergy Organ. J. 2016;9:9. doi: 10.1186/s40413-016-0101-8.
    1. Fiocchi A., Pawankar R., Cuello-Garcia C., Ahn K., Al-Hammadi S., Agarwal A., Beyer K., Burks W., Canonica G.W., Ebisawa M., et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics. World Allergy Organ. J. 2015;8:4. doi: 10.1186/s40413-015-0055-2.
    1. Underwood M.A. Should we treat every infant with a probiotic? Minerva. Pediatr. 2019;71:253–262. doi: 10.23736/S0026-4946.19.05526-9.
    1. Blauvelt A., de Bruin-Weller M., Gooderham M., Cather J.C., Weisman J., Pariser D., Simpson E.L., Papp K.A., Hong H.C., Rubel D., et al. Long-term management of moderate-to-severe atopic dermatitis with dupilumab and concomitant topical corticosteroids (LIBERTY AD CHRONOS): A 1-year, randomised, double-blinded, placebo-controlled, phase 3 trial. Lancet. 2017;389:2287–2303. doi: 10.1016/S0140-6736(17)31191-1.

Source: PubMed

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