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Supporting a Healthy Microbiome for the Primary Prevention of Eczema

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Abstract

Eczema is increasing worldwide with associated increases in health costs and decreases in quality of life. There are many factors that are speculated to interact in the development of eczema including genetics and environmental exposures. Prevention of the development of eczema may prevent the further development of food allergies and asthma. This concept has prompted a variety of research into the area of primary prevention of eczema in infants. This exploration includes a growing body of research examining infants supplemented with probiotics, prebiotics, or both (synbiotics) often compared with their breastfed counterparts. The goal of this paper is to examine the evidence for manipulating the microbiome in the prevention of eczema. Several strains of probiotics, compositions of prebiotics, and varied combinations of both are commercially available. Evidence supports altering the microbiome in infants at high risk of atopy who are not able to breastfeed with Lactobacillus strains when given both prenatally followed by prolonged use (greater than 6 months) postnatally for the primary prevention of eczema. Prebiotics have also been shown beneficial for primary prevention of eczema in formula-fed infants with prolonged use greater than 6 months. These findings are in keeping with the World Allergy Organization (WAO) recommendations that support interventions to manipulate the microbiome with both probiotics and prebiotics.

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Abbreviations

GI:

Gastrointestinal

OS:

Oligosaccharides

GOS:

Galacto-oligosaccharides

FOS:

Fructo-oligosaccharides

TLRs:

Toll-like receptors

DBRPC:

Double-blind, randomized, placebo controlled

SCFA:

Short-chain fatty acids

References

Introduction

  1. Martin PE et al (2013) The prevalence and socio-demographic risk factors of clinical eczema in infancy: a population-based observational study. Clin Exp Allergy 43(6):642–651

    CAS  PubMed  Google Scholar 

  2. Leung DY, Bieber T (2003) Atopic dermatitis. Lancet 361:151–160

    PubMed  Google Scholar 

  3. Lowe AJ, Leung DYM, Tang MLK et al (2018) The skin as a target for prevention of the atopic march. Ann Allergy Asthma Immunol 120(2):145–151

    PubMed  Google Scholar 

  4. Hoare C, Li Wan Po A, Williams H (2000) Systematic review of treatments for atopic eczema. Health Technol Assess 4(37):1–191

    CAS  PubMed  Google Scholar 

  5. “Microbiome.” Collegiate Dictionary. Merriam-Webster, 2018, unabridged. www.merriam-webster.com/dictionary/microbiome. Accessed 13 Aug 2019

  6. Moossavi S et al (2018) The prebiotic and probiotic properties of human milk: implications for infant immune development and pediatric asthma. Front Pediatr 6:197

    PubMed  Google Scholar 

  7. Bode L (2012) Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 22(9):1147–1162

    CAS  PubMed  Google Scholar 

  8. Thurl S, Munzert M, Boehm G et al (2017) Systematic review of the concentrations of oligosaccharides in human milk. Nutr Rev 75(11):920–933

    PubMed  Google Scholar 

  9. Ciaccio CE (2019) Modulating the microbiome. the future of allergy therapeutics? Ann Allergy Asthma Immunol 20(2):e77–e91 233–35

    Google Scholar 

  10. Smits HH, Engering A, van der Kleij D et al (2005) Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-brabbing nonintegrin. J Allergy Clin Immunol 115:1260–1267

    CAS  PubMed  Google Scholar 

  11. Lesiak A, Smolewski P, Sobolewska SD et al (2012) The role of T-regulatory cells and Toll-like receptors 2 and 4 in atopic dermatitis. Scand J Immunol 76:405–410

    CAS  PubMed  Google Scholar 

  12. Marlow G, Han DY, Wickens K et al (2015) Differential effects of two probiotics on the risks of eczema and atopy associated with single nucleotide polymorphisms to Toll-like receptors. Pediatr Allergy Immunol 26(3):262–271

    PubMed  Google Scholar 

  13. György P, Kuhn R, Rose CS, Zilliken F (1954a) bifidus factor I. A variant of Lactobacillus bifidus requiring a special growth factor. Arch Biochem Biophys 48:193–201

    PubMed  Google Scholar 

  14. György P, Kuhn R, Rose CS, Zilliken F (1954b) bifidus factor. II. Its occurrence in milk from different species and in other natural products. Arch Biochem Biophys 48:202–208

    PubMed  Google Scholar 

  15. György P, Hoover JR, Kuhn R, Rose CS (1954) Bifidus factor. III. The rate of dialysis. Arch Biochem Biophys 48:209–213

    PubMed  Google Scholar 

  16. Gauhe A, György P, Hoover JR et al (1954) Bifidus factor. IV. Preparations obtained from human milk. Arch Biochem Biophys 48:214–224

    CAS  PubMed  Google Scholar 

  17. Bode L (2015) The functional biology of human milk oligosaccharides. Early Hum Dev 91:619–622

    CAS  PubMed  Google Scholar 

  18. Ruiz-Palacios GM, Cervantes LE, Ramos P, Chavez-Munguia B, Newburg DS (2003) Campylobacter jejuni binds intestinal H (O) antigen (Fucα1,2Galβ1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J Biol Chem 278:14112–14120

    CAS  PubMed  Google Scholar 

  19. Manthey CF, Autran CA, Eckmann L, Bode L (2014) Human milk oligosaccharides protect against enteropathogenic E. coli attachment in vitro and colonization in suckling mice. J Pediatr Gastroenterol Nutr 58(2):167–170

    CAS  Google Scholar 

  20. Jantscher-Krenn E, Lauwaet T, Bliss LA, Reed SL, Gillin FD, Bode L (2012) Human milk oligosaccharides reduce Entamoeba histolytica attachment and cytotoxicity in vitro. Br J Nutr 108(10):1839–1846

    CAS  PubMed  Google Scholar 

  21. Angeloni S, Ridet JL, Kusy N et al (2005) Glycoprofiling with micro-arrays of glycoconjugates and lectins. Glycobiology 15:31–41

    CAS  PubMed  Google Scholar 

  22. Eiwegger T, Stahl B, Haidl P et al (2010) Prebiotic oligosaccharides: In vitro evidence for gastrointestinal epithelial transfer and immunomodulatory properties. Pediatr Allergy Immunol 21:1179–1188

    PubMed  Google Scholar 

  23. Vos AP, Haarman M, van Ginkel JW, Knol J, Garssen J, Stahl B et al (2007) Dietary supplementation of neutral and acidic oligosaccharides enhances Th1-dependent vaccination responses in mice. Pediatr Allergy Immunol 18:304–312

    PubMed  Google Scholar 

  24. Bode L, Kunz C, Muhly-Reinholz M, Mayer K, Seeger W, Rudloff S (2004) Inhibition of monocyte, lymphocyte, and neutrophil adhesion to endothelial cells by human milk oligosaccharides. Thromb Haemost 92:1402–1410

    CAS  PubMed  Google Scholar 

  25. Bode L, Rudloff S, Kunz C, Strobel S, Klein N (2004) Human milk oligosaccharides reduce platelet-neutrophil complex formation leading to a decrease in neutrophil β2 integrin expression. J Leukoc Biol 76:820–826

    CAS  PubMed  Google Scholar 

  26. Kong HDH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA et al (2012) Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22:850–859

    CAS  PubMed  Google Scholar 

  27. Nylund L, Satokari R, Nikkila J et al (2013) Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol 13:12

    PubMed  Google Scholar 

  28. Ismail IH, Oppedisano F, Joseph SJ et al (2012) Reduced gut microbial diversity in early life is associated with later development of eczema but not atopy in high-risk infants. Pediatr Allergy Immunol 23:674–681

    PubMed  Google Scholar 

  29. Abrahamsson TR, Jakobsson HE, Andersson AF et al (2012) Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 129:434–440 440 e431–432

    PubMed  Google Scholar 

  30. Wang M, Karlsson C, Olsson C et al (2008) Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol 121:129–134

    PubMed  Google Scholar 

  31. Okada H, Kuhn C, Feillet H, Bach JF (2010) The ‘hygiene hypothesis’ for autoimmune and allergic diseases: an update. Clin Exp Immunol 160:1–9

    CAS  PubMed  Google Scholar 

  32. Nakamizo S, Egawa G, Honda T, Nakajima S, Belkaid Y, Kabashima K (2015) Commensal bacteria and cutaneous immunity. Semin Immunopathol 37:73–80

    CAS  PubMed  Google Scholar 

Probiotics

  1. Kallioma M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E (2001) Probiotics in primary prevention of atopic disease: a randomized placebo-controlled trial. Lancet. 357(9262):1076–1079

    Google Scholar 

  2. Kallioma M, Salminen S, Poussa T, Arvilommi H, Isolauri E (2003) Probiotics and prevention of atopic disease: 4-year follow-up of a randomized placebo-controlled trial. Lancet. 361(9372):1869–1871

    Google Scholar 

  3. Kallioma M, Salminen S, Poussa T, Isolauri E (2007) Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. JACI

  4. Wickens K, Black PN, Stanley TV et al (2008) A differential effect of 2 probiotics in the prevention of eczema and atopy: a doubleblind, randomized, placebo-controlled trial. J Allergy Clin Immunol 788–94(22):122

    Google Scholar 

  5. Wickens K, Black P, Stanley TV, Mitchell E, Barthow C, Fitzharris P, Purdie G, Crane J (2012) A protective effect of Lactobacillus rhamnosus HN001 against eczema in the first 2 years of life persists to age 4 years. Clin Exp Allergy 42(7):1071–1079

    CAS  PubMed  Google Scholar 

  6. Wickens K, Stanley TV, Mitchell EA et al (2013) Early supplementation with Lactobacillus rhamnosus HN001 reduces eczema prevalence to 6 years: does it also reduce atopic sensitization? Clin Exp Allergy 43:1048–1057

    CAS  PubMed  Google Scholar 

  7. Morgan AR, Han DY, Wickens K, Barthow C, Mitchell EA, Stanley TV, Dekker J, Crane J, Ferguson LR (2014) Differential modification of genetic susceptibility to childhood eczema by two probiotics. Clin Exp Allergy 44(10):1255–1265

    CAS  PubMed  Google Scholar 

  8. Taylor AL, Dunstan JA, Prescott SL (2007) Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol 119(1):184–191

    PubMed  Google Scholar 

  9. Kopp MV, Hennemuth I, Heinzmann A, Urbanek R (2008) Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics. 121(4):e850–e856

    PubMed  Google Scholar 

  10. Soh SE, Aw M, Gerez I, Chong YS, Rauff M, Ng YP, Wong HB, Pai N, Lee BW, Shek LP (2009) Probiotic supplementation in the first 6 months of life in at risk Asian infants--effects on eczema and atopic sensitization at the age of 1 year. Clin Exp Allergy 39(4):571–578

    CAS  PubMed  Google Scholar 

  11. Allen SJ, Jordan S, Storey M, Thornton CA, Gravenor MB, Garaiova I, Plummer SF, Wang D, Morgan G (2014) Probiotics in the prevention of eczema: a randomised controlled trial. Arch Dis Child 99(11):1014–1019

    PubMed  Google Scholar 

  12. Cabana MD, McKean M, Caughey AB, Fong L, Lynch S, Wong A, Leong R, Boushey HA, Hilton JF (2017) Early probiotic supplementation for eczema and asthma prevention: a randomized controlled trial. Pediatrics. 140(3)

    PubMed  Google Scholar 

  13. Abrahamsson TR, Sinkiewicz G, Jakobsson T, Fredrikson M, Bjorksten B (2009) Probiotic lactobacilli in breast milk and infant stool in relation to oral intake during the first year of life. J Pediatr Gastroenterol Nutr 49:349–354

    PubMed  Google Scholar 

  14. Rautava S, Kainonen E, Salminen S, Isolauri E (2012) Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol 130(6):1355–1360

    CAS  PubMed  Google Scholar 

  15. Dotterud CK, Storro O, Johnsen R, Oien T (2010) Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. Br J Dermatol 163:616–623

    CAS  PubMed  Google Scholar 

  16. Kim JY, Kwon JH, Ahn SH, Lee SI, Han YS, Choi YO et al (2010) Effect of probiotic mix (Bifidobacterium bifidum, Bifidobacterium lactis, Lactobacillus acidophilus) in the primary prevention of eczema: a double-blind, randomized, placebocontrolled trial. Pediatr Allergy Immunol 21:e386–e393

    PubMed  Google Scholar 

  17. Wickens K, Barthow C, Mitchell EA, Stanley TV, Purdie G, Rowden J, Kang J, Hood F, van den Elsen L, Forbes-Blom E, Franklin I, Barnes P, Fitzharris P, Maude RM, Stone P, Abels P, Murphy R, Crane J (2018) Maternal supplementation alone with Lactobacillus rhamnosus HN001 during pregnancy and breastfeeding does not reduce infant eczema. Pediatr Allergy Immunol 29(3):296–302

    PubMed  Google Scholar 

  18. Osborn DA, Sinn JKH (2007) Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database of Systematic Reviews (4): CD006475.

  19. Lee J, Seto D, Bielory L (2008) Meta-analysis of clinical trials of probiotics for prevention and treatment of pediatric atopic dermatitis. J Allergy Clin Immunol 121:116–121

    PubMed  Google Scholar 

  20. Panduru M, Panduru NM, Sălăvăstru CM, Tiplica GS (2015) Probiotics and primary prevention of atopic dermatitis: a meta-analysis of randomized controlled studies. J Eur Acad Dermatol Venereol 29(2):232–242

    CAS  PubMed  Google Scholar 

  21. Cuello-Garcia CA, Brozek JL, Fiocchi A et al (2015) Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol 136:952–961

    PubMed  Google Scholar 

  22. Abbas A, Lichtman A, Pillai S. Cellular and molecular immunology. Elsevier. 2018. Print.

  23. Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A et al (2015) World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): probiotics. World Allergy Organ J 8:4

    PubMed  Google Scholar 

Prebiotics

  1. Boehm G, Lidestri M, Casetta P, Jelinek J, Negretti F, Stahl B, Marini A (2002) Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants. Arch Dis Child Fetal Neonatal Ed 86:F178–F181

    CAS  PubMed  Google Scholar 

  2. Moro G, Minoli I, Mosca M, Fanaro S, Jelinek J, Stahl B, Boehm G (2002) Dosage-related bifidogenic effects of galacto- and fructooligosaccharides in formula-fed term infants. J Pediatr Gastroenterol Nutr 34:291–295

    CAS  PubMed  Google Scholar 

  3. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G (2006) A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child 91:814–819

    CAS  PubMed  Google Scholar 

  4. Schmelzle H, Wirth S, Skopnik H, Radke M, Knol J, Bockler HM, Bronstrup A, Wells J, Fusch C (2003) Randomized double-blind study of the nutritional efficacy and bifidogenicity of a new infant formula containing partially hydrolyzed protein, a high beta-palmitic acid level, and nondigestible oligosaccharides. J Pediatr Gastroenterol Nutr 36:343–351

    CAS  PubMed  Google Scholar 

  5. Wopereis H, Sim K, Shaw A, Warner JO, Knol J, Kroll JS (2018) Intestinal microbiota in infants at high risk for allergy: Effects of prebiotics and role in eczema development. J Allergy Clin Immunol 141(4):1334–1342.e5

    CAS  PubMed  Google Scholar 

  6. Gruber C, van Stuijvenberg M, Mosca F et al (2010) Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among low-atopy-risk infants. J Allergy Clin Immunol 126:791–797

    PubMed  Google Scholar 

  7. Osborn DA, Sinn JK (2013) Prebiotics in infants for prevention of allergy. Cochrane Database Syst Rev 3:CD006474

    Google Scholar 

  8. Cuello-Garcia C, Fiocchi A, Pawankar R, Yepes-Nuñez JJ, Morgano GP, Zhang Y, Agarwal A, Gandhi S, Terracciano L, Schünemann HJ, Brozek JL (2017) Prebiotics for the prevention of allergies: a systematic review and meta-analysis of randomized controlled trials. Clin Exp Allergy 47(11):1468–1477

    CAS  PubMed  Google Scholar 

  9. Cuello-Garcia CA, Fiocchi A, Pawankar R et al (2016) World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): prebiotics. World Allergy Organ J 9:10

    PubMed  PubMed Central  Google Scholar 

Synbiotics

  1. Kukkonen K, Savilahti E, Haahtela T et al (2007) Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 119(1):192–198

    CAS  PubMed  Google Scholar 

  2. Rozé JC, Barbarot S, Butel MJ et al (2012) An α-lactalbumin-enriched and symbiotic-supplemented v. a standard infant formula: a multicentre, double-blind, randomized trial. Br J Nutr 107(11):1616–1622

    PubMed  Google Scholar 

  3. Chang YS, Trivedi MK, Jha A, Lin YF, Dimaano L, García-Romero MT (2016) Synbiotics for prevention and treatment of atopic dermatitis: a meta-analysis of randomized clinical trials. JAMA Pediatr 170(3):236–242

    PubMed  Google Scholar 

Conclusion

  1. Radbill S (1981) Infant feeding through the ages. Clin Pediatr 20(10):613–621

    CAS  Google Scholar 

  2. Stevens EE, Patrick TE, Pickler R (2009 Spring) A history of infant feeding. J Perinat Educ 18(2):32–39

    PubMed  PubMed Central  Google Scholar 

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  1. Department of Allergy-Immunology, Wilford Hall Ambulatory Surgical Center, Lackland Air Force Base, San Antonio, TX, USA

    Sofia Szari & James A. Quinn

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  1. Sofia Szari
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Correspondence to Sofia Szari.

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Szari, S., Quinn, J.A. Supporting a Healthy Microbiome for the Primary Prevention of Eczema. Clinic Rev Allerg Immunol 57, 286–293 (2019). https://doi.org/10.1007/s12016-019-08758-5

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