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Targeting Food Allergy with Probiotics

  • Lorella Paparo
  • Rita Nocerino
  • Carmen Di Scala
  • Giusy Della Gatta
  • Margherita Di Costanzo
  • Aniello Buono
  • Cristina Bruno
  • Roberto Berni CananiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series

Abstract

The dramatic increase in food allergy prevalence and severity globally is demanding effective strategies. Food allergy derives from a defect in immune tolerance mechanisms. Immune tolerance is modulated by gut microbiota composition and function, and gut microbiota dysbiosis has been associated with the development of food allergy. Selected probiotic strains could act on immune tolerance mechanisms. The mechanisms are multiple and still not completely defined. Increasing evidence is providing useful information on the choice of optimal bacterial species/strains, dosage, and timing for intervention. The increased knowledge on the crucial role played by gut microbiota-derived metabolites, such as butyrate, is also opening the way to a post-biotic approach in the stimulation of immune tolerance.

Keywords

Butyrate Cow’s milk allergy Gut microbiota Immune tolerance Post-biotics Probiotics 

Abbreviations

BLG

β-lactoglobulin

CMA

cow’s milk allergy

EHCF

extensively hydrolyzed casein formula

FA

food allergy

LAB

lactic acid bacteria

LGG

Lactobacillus rhamnosus GG

OIT

oral food immunotherapy

OVA

ovalbumin

PBMCs

peripheral blood mononuclear cells

SCFAs

short-chain fatty acids

SU

sustained unresponsiveness

Tregs

regulatory T cells

References

  1. Ai C, Ma N, Zhang Q et al (2016) Immunomodulatory effects of different lactic acid bacteria on allergic response and its relationship with in vitro properties. PLoS One 11:e0164697Google Scholar
  2. Aitoro R, Paparo L, Amoroso A et al (2017a) Gut microbiota as a target for preventive and therapeutic intervention against food allergy. Nutrients 9(7):pii: E672Google Scholar
  3. Aitoro R, Simeoli R, Amoroso A et al (2017b) Extensively hydrolyzed casein formula alone or with L. rhamnosus GG reduces β-lactoglobulin sensitization in mice. Pediatr Allergy Immunol 28:230–237Google Scholar
  4. Allen KJ, Koplin JJ (2016) Prospects for prevention of food allergy. J Allergy Clin Immunol Pract 4:215–220Google Scholar
  5. Arpaia N, Campbell C (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T cell generation. Nature 504:451–455Google Scholar
  6. Baldassarre ME, Laforgia N, Fanelli M et al (2010) Lactobacillus GG improves recovery in infants with blood in the stools and presumptive allergic colitis compared with extensively hydrolyzed formula alone. J Pediatr 156:397–401Google Scholar
  7. Ben-Shoshan M, Harrington DW, Soller L et al (2010) A population-based study on peanut, tree nut, fish, shellfish, and sesame allergy prevalence in Canada. J Allergy Clin Immunol 125:1327–1335Google Scholar
  8. Berin MC (2014) Future therapies for IgE mediated food allergy. Curr Pediatr Rep 2:119–126Google Scholar
  9. Berni Canani R, Nocerino R, Terrin G et al (2012a) Effect of Lactobacillus GG on tolerance acquisition in infants with cow’s milk allergy a randomized trial. J Allergy Clin Immunol 129:580–582; (582 e 1–5)Google Scholar
  10. Berni Canani R, Nocerino R, Terrin G et al (2012b) Effect of extensively hydrolyzed casein formula supplemented with Lactobacillus GG on tolerance acquisition in infants with cow’s milk allergy: a randomized trial. J Allergy Clin Immunol 129:580–582Google Scholar
  11. Berni Canani R, Nocerino R, Terrin G et al (2013) Formula selection for management of children with cow milk allergy influences the rate of acquisition of tolerance: a prospective multicenter study. J Pediatr 163:771–777Google Scholar
  12. Berni Canani R, Gilber JA, Nagler CR (2015) The role of the commensal microbiota in the regulation of tolerance to dietary allergens. Curr Opin Allergy Clin Immunol 15:243–249Google Scholar
  13. Berni Canani R, Sangwan N, Stefka AT et al (2016) Lactobacillus rhamnosus GG supplemented formula expands butyrate producing bacterial strains in food allergic infants. ISME J 10:742–750Google Scholar
  14. Berni Canani R, Di Costanzo M, Bedogni G et al (2017) Extensively hydrolyzed casein formula containing Lactobacillus rhamnosus GG reduces the occurrence of other allergic manifestation sin children with cow’s milk allergy: 3-year randomized controlled trial. J Allergy Clin Immunol 139:1906–1913Google Scholar
  15. Borchers AT, Keen CL, Gershwin ME (2002) The influence of yogurt/Lactobacillus on the innate and acquired immune response. Clin Rev Allergy Immunol 22:207–230Google Scholar
  16. Borthakur A, Gill RK, Tyagi S et al (2008) The probiotic Lactobacillus acidophilus stimulates chloride/hydroxyl exchange activity in human intestinal epithelial cells. J Nutr 138:1355–1359Google Scholar
  17. Boyce JA, Assa’ad A, Burks AW et al (2010) Guidelines for the diagnosis and management of food allergy in the United States: report of the NIAID-sponsored expert panel. J Allergy Clin Immunol 126:1105–1118Google Scholar
  18. Braat H, van den Brande J, van Tol E et al (2004) Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. Am J Clin Nutr 80:1618–1625Google Scholar
  19. Burks AW, Sampson HA, Plaut M et al (2018) Treatment for food allergy. J Allergy Clin Immunol 141:1–9Google Scholar
  20. Chafen JJ, Newberry SJ, Riedl MA et al (2010) Diagnosing and managing common food allergies: a systematic review. JAMA 303:1848–1856Google Scholar
  21. Cross ML, Gill HS (2001) Can immunoregulatory lactic acid bacteria be used as dietary supplements to limit allergies? Int Arch Allergy Immunol 125:112–119Google Scholar
  22. Di Costanzo M, Amoroso A, Berni Canani R et al (2016) Gut microbiota as a target for food allergy. J Pediatr Gastroenterol Nutr 63:S11–S13Google Scholar
  23. Donato KA, Gareau MG, Wang YJ (2010) Lactobacillus rhamnosus GG attenuates interferon-γ and tumor-necrosis factor-α- induced barrier dysfunction and pro-inflammatory signaling. Microbiology 156:3288–3297Google Scholar
  24. du Toit G, Sampson HA, Plaut M et al (2016) Prevention of food allergy. J Allergy Clin Immunol 137:998–1010Google Scholar
  25. Fiocchi A, Brozek J, Shunemann H et al (2010) World Allergy Organization (WAO) Diagnosis and Rationale for Action against Cow’s Milk Allergy (DRACMA) Guidelines. World Allergy Organ J 3:57–161Google Scholar
  26. Flinterman AE, Knol EF, van Ieperen AG et al (2007) Probiotics have a different immunomodulatory potential in vitro versus ex vivo upon oral administration in children with food allergy. Int Arch Allergy Immunol 143:237–244Google Scholar
  27. Furusawa Y, Obata Y (2013) Commensal microbe-derived butyrate induces differentiation of colonic regulatory T-cells. Nature 504:446–450Google Scholar
  28. Ghadimi D, Fölster-Holst R, de Vrese M et al (2008) Effects of probiotic bacteria and their genomic DNA on TH1/TH2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunobiology 213:677–692Google Scholar
  29. Ghadimi D, Helwig U, Schrezenmeir J et al (2012) Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. J Leukoc Biol 92:895–911Google Scholar
  30. Gupta RS, Springston EE, Warrier MR et al (2011) The prevalence, severity, and distribution of childhood food allergy in the United States. Pediatrics 128:e9–e17Google Scholar
  31. Gupta R, Holdford D, Bilaver L et al (2013) The economic impact of childhood food allergy in the United States. JAMA Pediatr 167:1026–1031Google Scholar
  32. Gupta RS, Walkner MM, Greenhawt M et al (2016) Food allergy sensitization and presentation in siblings of food allergic children. J Allergy Clin Immunol Pract 4:956–962Google Scholar
  33. Hardy H, Harris J, Lyon W et al (2013) Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5:1869–1912Google Scholar
  34. Heine RG (2018) Food allergy prevention and treatment by targeted nutrition. Ann Nutr Metab 72:27–39Google Scholar
  35. Hill C, Guarner F, Reid G et al (2014) Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514Google Scholar
  36. Ho H, Bunyavanich S (2018) Role of the microbiome in food allergy. Curr Allergy Asthma Rep 18:27Google Scholar
  37. Hol J, van Leer EH, Elink Schuurman BE et al (2008) The acquisition of tolerance towards cow’s milk through probiotic supplementation: a randomized controlled trial. J Allergy Clin Immunol 121:1448–1454Google Scholar
  38. Hong X, Hao K, Ladd-Acosta C et al (2015) Genome-wide association study identifies peanut allergy-specific loci and evidence of epigenetic mediation in US children. Nat Commun 6:6304Google Scholar
  39. Huang YJ, Marsland BJ, Bunyavanich S et al (2017) The microbiome in allergic disease: current understanding and future opportunities—2017 PRACTALL document of the American Academy of Allergy, Asthma & Immunology and the European Academy of Allergy and Clinical Immunology. J Allergy Clin Immunol 139:1099–1110Google Scholar
  40. Isolauri E, Arvola T, Sutas Y et al (2000) Probiotics in the management of atopic eczema. Clin Exp Allergy 30:1604–1161Google Scholar
  41. Juan Z, Hui S, Qiuhong L et al (2017) Oral administration of Clostridium butyricum CGMCC0313.1 inhibits β-lactoglobulin-induced intestinal anaphylaxis in a mouse model of food allergy. Gut Pathogens 9:11Google Scholar
  42. Karlsson H, Larsson P, Wold AE et al (2004) Pattern of cytokine responses to Gram-positive and Gram-negative commensal bacteria is profoundly changed when monocytes differentiate into dendritic cells. Infect Immun 72:2671–2678Google Scholar
  43. Kim JY, Choi YO, GE J (2008) Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J Microbiol Biotechnol 18:1393–1400Google Scholar
  44. Kukkonen K, Savilahti E, Haahtela T et al (2007) Probiotics and prebiotic galactooligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 119:192–198Google Scholar
  45. Linglin F, Jixiang P, Shushu Z et al (2017) Lactic acid bacteria-specific induction of CD4+Foxp3+T cells ameliorates shrimp tropomyosin induced allergic response in mice via suppression of mTOR signaling. Sci Rep 7:1987Google Scholar
  46. Maassen CB, van Holten-Neelen C, Balk F et al (2000) Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18:2613–2623Google Scholar
  47. Maiga MA, Morin S, Bernard H et al (2017) Neonatal mono-colonization of germ-free mice with Lactobacillus casei enhances casein immunogenicity after oral sensitization to cow’s milk. Mol Nutr Food Res 61:10–1002Google Scholar
  48. Malin M, Verronen P, Korhonen H et al (1997) Dietary therapy with Lactobacillus GG, bovine colostrum or bovine immune colostrum in patients with juvenile chronic arthritis: evaluation of effect on gut defence mechanisms. Inflammopharmacology 5:219–236Google Scholar
  49. McBride D, Keil T, Grabenhenrich L et al (2012) The EuroPrevall birth cohort study on food allergy: baseline characteristics of 12,000 newborns and their families from nine European countries. Pediatr Allergy Immunol 23:230–239Google Scholar
  50. Meng-Yun L, Zhen-Yu Y, Wen-Kui D et al (2017) Protective effect of Bifidobacterium infantis CGMCC313-2 on ovalbumin-induced airway asthma and b-lactoglobulininduced intestinal food allergy mouse models. World J Gastroenterol 23:2149–2158Google Scholar
  51. Mileti E, Matteoli G, Iliev D et al (2009) Comparison of the immunomodulatory properties of three probiotics strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS One 4:e7056Google Scholar
  52. Mohamadzadeh M, Olson S, Kalina WV et al (2005) Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A 102:2880–2885Google Scholar
  53. Mullins RJ, Dear KB, Tang ML (2015) Time trends in Australian hospital anaphylaxis admissions in 1998–1999 to 2011–2012. J Allergy Clin Immunol 136:367–375Google Scholar
  54. Mullins RJ, Wainstein BK, Barnes EH et al (2016) Increases in anaphylaxis fatalities in Australia from 1997 to 2013. Clin Exp Allergy 46:1099–1110Google Scholar
  55. National Academies of Sciences (2016) Engineering and Medicine. Finding a path to safety in food allergy: assessment of global burden, causes, prevention, management, and public policy. National Academies of Sciences, Engineering and Medicine, Washington, DCGoogle Scholar
  56. Niers LE, Timmerman HM, Rijkers GT et al (2005) Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy 35:1481–1489Google Scholar
  57. Nocerino R, Leone L, Cosenza L et al (2015) Increasing rate of hospitalizations for food-induced anaphylaxis in Italian children: an analysis of the Italian Ministry of Health database. J Allergy Clin Immunol 135:833–835.e3Google Scholar
  58. Nowak-Wegrzyn A, Chatchatee P (2017) Mechanisms of tolerance induction. Ann Nutr Metab 70:7–24Google Scholar
  59. Osborne NJ, Koplin JJ, Martin PE et al (2011) Prevalence of challenge-proven IgE-mediated food allergy using population-based sampling and predetermined challenge criteria in infants. J Allergy Clin Immunol 127:668–676.e2Google Scholar
  60. Pan SJ, Kuo CH, Lam KP (2010) Probiotics and allergy in infants -an update review. Pediatr Allergy Immunol 21:e659–e666Google Scholar
  61. Paparo L, Aitoro R, Nocerino R et al (2018) Epigenetic regulation of early nutrition on immune system. In: Preedy VR, Patel VB (eds) Handbook of nutrition, diet, and epigenetics. Springer, Cham.  https://doi.org/10.1007/978-3-319-31143-2_54-1CrossRefGoogle Scholar
  62. Prince BT, Mandel MJ, Nadeau K et al (2015) Gut microbiome and the development of food allergy and allergic disease. Pediatr Clin North Am 62:1479:92Google Scholar
  63. Rachid R, Keet CA (2018) Current status and unanswered questions for food allergy treatments. J Allergy Clin Immunol Pract 6:377–382Google Scholar
  64. Ramesh M, Yuenyongviwat A, Kostantinou GN et al (2016) Peanut T-cell epitope discovery: Ara h 1. J Allergy Clin Immunol 137:1764–1771.e4Google Scholar
  65. Rautava S, Collado MC, Salminen S et al (2012) Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102:178–184Google Scholar
  66. Sandin A, Bråbäck L, Norin E et al (2009) Faecal short chain fatty acid pattern and allergy in early childhood. Acta Paediatr 98:823–827Google Scholar
  67. Savage J, Sicherer S, Wood R (2016) The natural history of food allergy. J Allergy Clin Immunol Pract 4:196–203Google Scholar
  68. Savage JH, Lee-Sarwar KA, Sordillo J et al (2018) A prospective microbiome-wide association study of food sensitization and food allergy in early childhood. Allergy 73(1):145–152Google Scholar
  69. Schiavi E, Barletta B, Butteroni C et al (2011) Oral therapeutic administration of a probiotic mixture suppresses established Th2 responses and systemic anaphylaxis in a murine model of food allergy. Allergy 66:499–508Google Scholar
  70. Sicherer SH, Sampson HA (2018) Food allergy: a review and update on epidemiology, pathogenesis, diagnosis, prevention, and management. J Allergy Clin Immunol 141:41–48Google Scholar
  71. Sicherer SH, Munoz-Furlong A, Godbold JH et al (2010) US prevalence of self-reported peanut, tree nut, and sesame allergy: 11-year follow-up. J Allergy Clin Immunol 125:1322–1326Google Scholar
  72. Sicherer SH, Wood RA, Vickery BP et al (2014) The natural history of milk allergy in an observational cohort. J Allergy Clin Immunol 133:492–498Google Scholar
  73. Sicherer SH, Allen K, Lack G et al (2017) Critical issues in food allergy: a national academies consensus report. Pediatrics 24:e20170194Google Scholar
  74. Skripak JM, Matsui EC, Mudd K et al (2007) The natural history of IgE-mediated cow’s milk allergy. J Allergy Clin Immunol 120:1172–1177Google Scholar
  75. Smith PM, Howitt MR (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573Google Scholar
  76. 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-grabbing nonintegrin. J Allergy Clin Immunol 115:1260–1267Google Scholar
  77. Sudo N, Sawamura S, Tanaka K et al (1997) The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 159:1739–1745Google Scholar
  78. Sütas Y, Hurme M, Isolauri E (1996) Down-regulation of anti-CD3 antibody-induced IL-4 production by bovine caseins hydrolysed with Lactobacillus GG-derived enzymes. Scand J Immunol 43:687–689Google Scholar
  79. Takahashi S, Kawamura T, Kanda Y et al (2006a) Activation of CD1d-independent NK1.1+ T cells in the large intestine by Lactobacilli. Immunol Lett 102:74–78Google Scholar
  80. Takahashi N, Kitazawa H, Iwabuchi N et al (2006b) Oral administration of an immunostimulatory DNA sequence from Bifidobacterium longum improves Th1/Th2 balance in a murine model. Biosci Biotechnol Biochem 70:2013–2017Google Scholar
  81. Tan J, McKenzie C, Vuillermin PJ et al (2016) Dietary fiber and bacterial SCFA enhance oral tolerance and protect against food allergy through diverse cellular pathways. Cell Rep 15:2809–2824Google Scholar
  82. Tang ML, Ponsonby AL, Orsini F et al (2015) Administration of a probiotic with peanut oral immunotherapy: a randomized trial. J Allergy Clin Immunol 135:737–744Google Scholar
  83. Tao R, de Zoeten EF (2007) Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 13:1299–1307Google Scholar
  84. Thang CL, Baurhoo B, Boye JI et al (2011) Effects of Lactobacillus rhamnosus GG supplementation on cow’s milk allergy in a mouse model. Allergy Asthma Clin Immunol 6:7–20Google Scholar
  85. Torii A, Torii S, Fujiwara S et al (2007) Lactobacillus Acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol Int 56:293–301Google Scholar
  86. Turner PJ, Gowland MH, Sharma V et al (2015) Increase in anaphylaxis-related hospitalizations but no increase in fatalities: an analysis of United Kingdom national anaphylaxis data, 1992–2012. J Allergy Clin Immunol 135:956–63.e1Google Scholar
  87. Viljanen M, Savilahti E, Haahtela T et al (2005) Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo controlled trial. Allergy 60:494–500Google Scholar
  88. Wang J, Tang H, Zhang C et al (2015) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J 9(1):1–15Google Scholar
  89. Wood RA, Sicherer SH, Vickery BP et al (2013) The natural history of milk allergy in an observational cohort. J Allergy Clin Immunol 131:805–812.e4Google Scholar
  90. Wu YJ, Wu WF, Hang CW et al (2017) 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 50:684–692Google Scholar
  91. Yang B, Xiao L, Liu S et al (2017) Exploration of the effect of probiotics supplementation on intestinal microbiota of food allergic mice. Am J Transl Res 9:376–385Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Lorella Paparo
    • 1
    • 3
  • Rita Nocerino
    • 1
    • 3
  • Carmen Di Scala
    • 1
    • 3
  • Giusy Della Gatta
    • 1
    • 3
  • Margherita Di Costanzo
    • 1
    • 3
  • Aniello Buono
    • 3
  • Cristina Bruno
    • 1
  • Roberto Berni Canani
    • 1
    • 2
    • 3
    • 4
    Email author
  1. 1.Department of Translational Medical ScienceUniversity of Naples “Federico II”NaplesItaly
  2. 2.European Laboratory for the Investigation of Food-Induced DiseasesUniversity of Naples “Federico II”NaplesItaly
  3. 3.CEINGE-Biotecnologie Avanzate s.c.ar.l.University of Naples “Federico II”NaplesItaly
  4. 4.Task Force on Microbiome InvestigationUniversity of Naples Federico IINaplesItaly

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