Bugging allergy; role of pre-, pro- and synbiotics in allergy prevention

Allergology International

Volumn 66, Issue 4, 2017, Pages 529-538

  West, Christina E ^a,b   Dzidic, Majda ^b,c,d   Prescott, Susan L ^b,e   Jenmalm, Maria C ^b,c  

^a UMEÅ UNIVERSITY   (Sweden)

^b inFLAME Global Network (Worldwide Universities Network)   (United States)

^c LINKÖPING UNIVERSITY   (Sweden)

^d INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^e PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

Author keywords

Asthma; Biodiversity; Eczema; Microbiome; Probiotic

Indexed keywords

FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; OLIGOSACCHARIDE; PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; SECRETORY IMMUNOGLOBULIN; SYNBIOTIC AGENT;

ADAPTIVE IMMUNITY; ALLERGIC ASTHMA; ALLERGIC RHINITIS; ALLERGY; ASTHMA; ATOPIC DERMATITIS; ATOPY; CLINICAL RESEARCH; DIETARY INTAKE; DYSBIOSIS; ECZEMA; FOOD ALLERGY; HUMAN; IMMUNOCOMPETENCE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE FLORA; LIFESTYLE; LONG TERM CARE; MICROBIOME; NATIONAL HEALTH ORGANIZATION; PRACTICE GUIDELINE; PREVENTIVE MEDICINE; PRIMARY PREVENTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; RESPIRATORY TRACT ALLERGY; REVIEW; RISK FACTOR; SKIN ALLERGY; SYSTEMATIC REVIEW; WHEEZING; ANIMAL; CLINICAL STUDY; HYPERSENSITIVITY; IMMUNITY; IMMUNOLOGY; MICROFLORA; OUTCOME ASSESSMENT;

ANIMALS; CLINICAL STUDIES AS TOPIC; HUMANS; HYPERSENSITIVITY; IMMUNE TOLERANCE; IMMUNITY; IMMUNOMODULATION; MICROBIOTA; OUTCOME ASSESSMENT (HEALTH CARE); PREBIOTICS; PROBIOTICS; SYNBIOTICS;

EID: 85028625251     PISSN: 13238930     EISSN: 14401592     Source Type: Journal    
DOI: 10.1016/j.alit.2017.08.001     Document Type: Review

References (141)

1. Hanski, I., von Hertzen, L., Fyhrquist, N., Koskinen, K., Torppa, K., Laatikainen, T., et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A 109 (2012), 8334–8339.
2. Haahtela, T., Holgate, S., Pawankar, R., Akdis, C.A., Benjaponpitak, S., Caraballo, L., et al. The biodiversity hypothesis and allergic disease: world allergy organization position statement. World Allergy Organ J, 6, 2013, 3.
3. West, C.E., Renz, H., Jenmalm, M.C., Kozyrskyj, A.L., Allen, K.J., Vuillermin, P., et al. The gut microbiota and inflammatory noncommunicable diseases: associations and potentials for gut microbiota therapies. J Allergy Clin Immunol 135 (2015), 3–13.
4. Logan, A.C., Dysbiotic drift: mental health, environmental grey space, and microbiota. J Physiol Anthropol, 34, 2015, 23.
5. Prescott, S.L., Logan, A.C., Millstein, R.A., Katszman, M.A., Biodiversity, the human microbiome and mental health: moving toward a new clinical ecology for the 21st century?. Int J Biodivers, 2016, 10.1155/2016/2718275.
6. Prescott, S.L., Logan, A.C., The Secret Life of Your Microbiome. Why Nature and Biodiversity are Essential to Health and Happiness. 2017, New Society Publishers, Canada.
7. Prescott, S.L., Logan, A.C., Transforming life: a broad view of the developmental origins of health and disease concept from an ecological justice perspective. Int J Environ Res Public Health, 13, 2016.
8. West, C.E., Jenmalm, M.C., Prescott, S.L., The gut microbiota and its role in the development of allergic disease: a wider perspective. Clin Exp Allergy 45 (2015), 43–53.
9. Kalliomäki, M., Kirjavainen, P., Eerola, E., Kero, P., Salminen, S., Isolauri, E., Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 107 (2001), 129–134.
10. Penders, J., Thijs, C., van den Brandt, P.A., Kummeling, I., Snijders, B., Stelma, F., et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56 (2007), 661–667.
11. Sjögren, Y.M., Jenmalm, M.C., Böttcher, M.F., Björkstén, B., Sverremark-Ekström, E., Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy 39 (2009), 518–526.
12. Bisgaard, H., Li, N., Bonnelykke, K., Chawes, B.L., Skov, T., Paludan-Muller, G., et al. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol, 128, 2011 646–52.e1–5.
13. Abrahamsson, T.R., Jakobsson, H.E., Andersson, A.F., Björkstén, B., Engstrand, L., Jenmalm, M.C., Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 129 (2012), 434–440 40e1–2.
14. Ismail, I.H., Oppedisano, F., Joseph, S.J., Boyle, R.J., Licciardi, P.V., Robins-Browne, R.M., et al. 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 (2012), 674–681.
15. Penders, J., Gerhold, K., Stobberingh, E.E., Thijs, C., Zimmermann, K., Lau, S., et al. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol, 132, 2013 601–607. e8.
16. Abrahamsson, T.R., Jakobsson, H.E., Andersson, A.F., Björkstén, B., Engstrand, L., Jenmalm, M.C., Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy 44 (2014), 842–850.
17. West, C.E., Rydén, P., Lundin, D., Engstrand, L., Tulic, M.K., Prescott, S.L., Gut microbiome and innate immune response patterns in IgE-associated eczema. Clin Exp Allergy 45 (2015), 1419–1429.
18. Arrieta, M.C., Stiemsma, L.T., Dimitriu, P.A., Thorson, L., Russell, S., Yurist-Doutsch, S., et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med, 7, 2015 307ra152.
19. Stiemsma, L.T., Arrieta, M.C., Dimitriu, P.A., Cheng, J., Thorson, L., Lefebvre, D.L., et al. Shifts in Lachnospira and Clostridium sp. in the 3-month stool microbiome are associated with preschool age asthma. Clin Sci (Lond) 130 (2016), 2199–2207.
20. Fujimura, K.E., Sitarik, A.R., Havstad, S., Lin, D.L., Levan, S., Fadrosh, D., et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med 22 (2016), 1187–1191.
21. Food and Agriculture Organization WHOFW, Report of Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria., 2001.
22. Gibson, G.R., Hutkins, R., Sanders, M.E., Prescott, S.L., Reimer, R.A., Salminen, S.J., et al. Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14 (2017), 491–502.
23. Rodriguez, J.M., Murphy, K., Stanton, C., Ross, R.P., Kober, O.I., Juge, N., et al. The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis, 26, 2015, 26050.
24. Yu, W., Freeland, D.M., Nadeau, K.C., Food allergy: immune mechanisms, diagnosis and immunotherapy. Nat Rev Immunol 16 (2016), 751–765.
25. Blazquez, A.B., Berin, M.C., Microbiome and food allergy. Transl Res 179 (2017), 199–203.
26. Wang, M., Karlsson, C., Olsson, C., Adlerberth, I., Wold, A.E., Strachan, D.P., et al. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J Allergy Clin Immunol 121 (2008), 129–134.
27. Azad, M.B., Konya, T., Guttman, D.S., Field, C.J., Sears, M.R., HayGlass, K.T., et al. Infant gut microbiota and food sensitization: associations in the first year of life. Clin Exp Allergy 45 (2015), 632–643.
28. Bunyavanich, S., Shen, N., Grishin, A., Wood, R., Burks, W., Dawson, P., et al. Early-life gut microbiome composition and milk allergy resolution. J Allergy Clin Immunol 138 (2016), 1122–1130.
29. Wesemann, D.R., Nagler, C.R., The microbiome, timing, and barrier function in the context of allergic disease. Immunity 44 (2016), 728–738.
30. Stefka, A.T., Feehley, T., Tripathi, P., Qiu, J., McCoy, K., Mazmanian, S.K., et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci U S A 111 (2014), 13145–13150.
31. Pabst, O., Cerovic, V., Hornef, M., Secretory IgA in the coordination of establishment and maintenance of the microbiota. Trends Immunol 37 (2016), 287–296.
32. Pabst, O., New concepts in the generation and functions of IgA. Nat Rev Immunol 12 (2012), 821–832.
33. Dzidic, M., Abrahamsson, T.R., Artacho, A., Björkstén, B., Collado, M.C., Mira, A., et al. Aberrant IgA responses to the gut microbiota during infancy precede asthma and allergy development. J Allergy Clin Immunol, 139, 2017 1017–1025. e14.
34. Wesemann, D.R., Portuguese, A.J., Meyers, R.M., Gallagher, M.P., Cluff-Jones, K., Magee, J.M., et al. Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 501 (2013), 112–115.
35. Rodriguez, B., Prioult, G., Hacini-Rachinel, F., Moine, D., Bruttin, A., Ngom-Bru, C., et al. Infant gut microbiota is protective against cow's milk allergy in mice despite immature ileal T-cell response. FEMS Microbiol Ecol 79 (2012), 192–202.
36. West, C.E., Jenmalm, M.C., Kozyrskyj, A.L., Prescott, S.L., Probiotics for treatment and primary prevention of allergic diseases and asthma: looking back and moving forward. Expert Rev Clin Immunol 12 (2016), 625–639.
37. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331 (2011), 337–341.
38. Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500 (2013), 232–236.
39. Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9 (2009), 313–323.
40. Sabat, R., Ouyang, W., Wolk, K., Therapeutic opportunities of the IL-22-IL-22R1 system. Nat Rev Drug Discov 13 (2014), 21–38.
41. Round, J.L., Mazmanian, S.K., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 107 (2010), 12204–12209.
42. Bashir, M.E., Louie, S., Shi, H.N., Nagler-Anderson, C., Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J Immunol 172 (2004), 6978–6987.
43. Noval Rivas, M., Burton, O.T., Wise, P., Zhang, Y.Q., Hobson, S.A., Garcia Lloret, M., et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol 131 (2013), 201–212.
44. Arpaia, N., Rudensky, A.Y., Microbial metabolites control gut inflammatory responses. Proc Natl Acad Sci U S A 111 (2014), 2058–2059.
45. Furusawa, Y., Obata, Y., Fukuda, S., Endo, T.A., Nakato, G., Takahashi, D., et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504 (2013), 446–450.
46. Smith, P.M., Howitt, M.R., Panikov, N., Michaud, M., Gallini, C.A., Bohlooly, Y.M., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341 (2013), 569–573.
47. Chang, P.V., Hao, L., Offermanns, S., Medzhitov, R., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A 111 (2014), 2247–2252.
48. Boyle, R.J., Ismail, I.H., Kivivuori, S., Licciardi, P.V., Robins-Browne, R.M., Mah, L.J., et al. Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial. Allergy 66 (2011), 509–516.
49. Dotterud, C.K., Storro, O., Johnsen, R., Oien, T., Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. Br J Dermatol 163 (2010), 616–623.
50. Rautava, S., Kainonen, E., Salminen, S., Isolauri, E., Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol 130 (2012), 1355–1360.
51. Ou, C.Y., Kuo, H.C., Wang, L., Hsu, T.Y., Chuang, H., Liu, C.A., et al. Prenatal and postnatal probiotics reduces maternal but not childhood allergic diseases: a randomized, double-blind, placebo-controlled trial. Clin Exp Allergy 42 (2012), 1386–1396.
52. Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., Isolauri, E., Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 357 (2001), 1076–1079.
53. Kopp, M.V., Hennemuth, I., Heinzmann, A., Urbanek, R., Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics 121 (2008), e850–e856.
54. Kukkonen, K., Savilahti, E., Haahtela, T., Juntunen-Backman, K., Korpela, R., Poussa, T., et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 119 (2007), 192–198.
55. Abrahamsson, T.R., Jakobsson, T., Böttcher, M.F., Fredrikson, M., Jenmalm, M.C., Björkstén, B., et al. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 119 (2007), 1174–1180.
56. Wickens, K., Black, P.N., Stanley, T.V., Mitchell, E., Fitzharris, P., Tannock, G.W., et al. A differential effect of 2 probiotics in the prevention of eczema and atopy: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 122 (2008), 788–794.
57. Huurre, A., Laitinen, K., Rautava, S., Korkeamäki, M., Isolauri, E., Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy 38 (2008), 1342–1348.
58. Niers, L., Martin, R., Rijkers, G., Sengers, F., Timmerman, H., van Uden, N., et al. The effects of selected probiotic strains on the development of eczema (the PandA study). Allergy 64 (2009), 1349–1358.
59. Kim, J.Y., Kwon, J.H., Ahn, S.H., Lee, S.I., Han, Y.S., Choi, Y.O., et al. 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 21 (2010), e386–e393.
60. Allen, S.J., Jordan, S., Storey, M., Thornton, C.A., Gravenor, M.B., Garaiova, I., et al. Probiotics in the prevention of eczema: a randomised controlled trial. Arch Dis Child 99 (2014), 1014–1019.
61. Taylor, A.L., Dunstan, J.A., Prescott, S.L., 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 (2007), 184–191.
62. Soh, S.E., Aw, M., Gerez, I., Chong, Y.S., Rauff, M., Ng, Y.P., et al. 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 (2009), 571–578.
63. West, C.E., Hammarström, M.L., Hernell, O., Probiotics during weaning reduce the incidence of eczema. Pediatr Allergy Immunol 20 (2009), 430–437.
64. Simpson, M.R., Dotterud, C.K., Storro, O., Johnsen, R., Oien, T., Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial. BMC Dermatol, 15, 2015, 13.
65. Kalliomäki, M., Salminen, S., Poussa, T., Isolauri, E., Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. J Allergy Clin Immunol 119 (2007), 1019–1021.
66. Kuitunen, M., Kukkonen, K., Juntunen-Backman, K., Korpela, R., Poussa, T., Tuure, T., et al. Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. J Allergy Clin Immunol 123 (2009), 335–341.
67. Abrahamsson, T.R., Jakobsson, T., Björkstén, B., Oldaeus, G., Jenmalm, M.C., No effect of probiotics on respiratory allergies: a seven-year follow-up of a randomized controlled trial in infancy. Pediatr Allergy Immunol 24 (2013), 556–561.
68. Wickens, K., Stanley, T.V., Mitchell, E.A., Barthow, C., Fitzharris, P., Purdie, G., et al. Early supplementation with Lactobacillus rhamnosus HN001 reduces eczema prevalence to 6 years: does it also reduce atopic sensitization?. Clin Exp Allergy 43 (2013), 1048–1057.
69. Jensen, M.P., Meldrum, S., Taylor, A.L., Dunstan, J.A., Prescott, S.L., Early probiotic supplementation for allergy prevention: long-term outcomes. J Allergy Clin Immunol 130 (2012), 1209–1211 e5.
70. Loo, E.X., Llanora, G.V., Lu, Q., Aw, M.M., Lee, B.W., Shek, L.P., Supplementation with probiotics in the first 6 months of life did not protect against eczema and allergy in at-risk Asian infants: a 5-year follow-up. Int Arch Allergy Immunol 163 (2014), 25–28.
71. West, C.E., Hammarström, M.L., Hernell, O., Probiotics in primary prevention of allergic disease – follow-up at 8-9 years of age. Allergy 68 (2013), 1015–1020.
72. Gorissen, D.M., Rutten, N.B., Oostermeijer, C.M., Niers, L.E., Hoekstra, M.O., Rijkers, G.T., et al. Preventive effects of selected probiotic strains on the development of asthma and allergic rhinitis in childhood. The Panda study. Clin Exp Allergy 44 (2014), 1431–1433.
73. Peldan, P., Kukkonen, A.K., Savilahti, E., Kuitunen, M., Perinatal probiotics decreased eczema up to 10 years of age, but at 5–10 years, allergic rhino-conjunctivitis was increased. Clin Exp Allergy 47 (2017), 975–979.
74. Lundelin, K., Poussa, T., Salminen, S., Isolauri, E., Long-term safety and efficacy of perinatal probiotic intervention: evidence from a follow-up study of four randomized, double-blind, placebo-controlled trials. Pediatr Allergy Immunol 28 (2017), 170–175.
75. Cuello-Garcia, C.A., Brozek, J.L., Fiocchi, A., Pawankar, R., Yepes-Nunez, J.J., Terracciano, L., et al. Probiotics for the prevention of allergy: a systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol 136 (2015), 952–961.
76. Zuccotti, G., Meneghin, F., Aceti, A., Barone, G., Callegari, M.L., Di Mauro, A., et al. Probiotics for prevention of atopic diseases in infants: systematic review and meta-analysis. Allergy 70 (2015), 1356–1371.
77. Zhang, G.Q., Hu, H.J., Liu, C.Y., Zhang, Q., Shakya, S., Li, Z.Y., Probiotics for prevention of atopy and food hypersensitivity in early childhood: a PRISMA-compliant systematic review and meta-analysis of randomized controlled trials. Medicine (Baltimore), 95, 2016, e2562.
78. Azad, M.B., Coneys, J.G., Kozyrskyj, A.L., Field, C.J., Ramsey, C.D., Becker, A.B., et al. Probiotic supplementation during pregnancy or infancy for the prevention of asthma and wheeze: systematic review and meta-analysis. BMJ, 347, 2013, f6471.
79. Kalliomäki, M., Salminen, S., Poussa, T., Arvilommi, H., Isolauri, E., Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. Lancet 361 (2003), 1869–1871.
80. Forsberg, A., West, C.E., Prescott, S.L., Jenmalm, M.C., Pre- and probiotics for allergy prevention: time to revisit recommendations?. Clin Exp Allergy 46 (2016), 1506–1521.
81. Bode, L., The functional biology of human milk oligosaccharides. Early Hum Dev 91 (2015), 619–622.
82. Cuello-Garcia, C.A., Fiocchi, A., Pawankar, R., Yepes-Nunez, J.J., Morgano, G.P., Zhang, Y., et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): prebiotics. World Allergy Organ J, 9, 2016, 10.
83. Roze, J.C., Barbarot, S., Butel, M.J., Kapel, N., Waligora-Dupriet, A.J., De Montgolfier, I., et al. An alpha-lactalbumin-enriched and symbiotic-supplemented v. a standard infant formula: a multicentre, double-blind, randomised trial. Br J Nutr 107 (2012), 1616–1622.
84. Chang, Y.S., Trivedi, M.K., Jha, A., Lin, Y.F., Dimaano, L., Garcia-Romero, M.T., Synbiotics for prevention and treatment of atopic dermatitis: a meta-analysis of randomized clinical trials. JAMA Pediatr 170 (2016), 236–242.
85. Jenmalm, M.C., Duchen, K., Timing of allergy-preventive and immunomodulatory dietary interventions – are prenatal, perinatal or postnatal strategies optimal?. Clin Exp Allergy 43 (2013), 273–278.
86. Frei, R., Akdis, M., O'Mahony, L., Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence. Curr Opin Gastroenterol 31 (2015), 153–158.
87. Wilson, C.B., Westall, J., Johnston, L., Lewis, D.B., Dower, S.K., Alpert, A.R., Decreased production of interferon-gamma by human neonatal cells. Intrinsic and regulatory deficiencies. J Clin Invest 77 (1986), 860–867.
88. White, G.P., Watt, P.M., Holt, B.J., Holt, P.G., Differential patterns of methylation of the IFN-gamma promoter at CpG and non-CpG sites underlie differences in IFN-gamma gene expression between human neonatal and adult CD45RO- T cells. J Immunol 168 (2002), 2820–2827.
89. Krumbiegel, D., Zepp, F., Meyer, C.U., Combined Toll-like receptor agonists synergistically increase production of inflammatory cytokines in human neonatal dendritic cells. Hum Immunol 68 (2007), 813–822.
90. Abrahamsson, T.R., Sandberg Abelius, M., Forsberg, A., Björkstén, B., Jenmalm, M.C., A Th1/Th2-associated chemokine imbalance during infancy in children developing eczema, wheeze and sensitization. Clin Exp Allergy 41 (2011), 1729–1739.
91. Gollwitzer, E.S., Marsland, B.J., Impact of early-life exposures on immune maturation and susceptibility to disease. Trends Immunol 36 (2015), 684–696.
92. Kollmann, T.R., Kampmann, B., Mazmanian, S.K., Marchant, A., Levy, O., Protecting the newborn and young infant from infectious diseases: lessons from immune ontogeny. Immunity 46 (2017), 350–363.
93. Jenmalm, M.C., Childhood immune maturation and allergy development: regulation by maternal immunity and microbial exposure. Am J Reprod Immunol 66:Suppl 1 (2011), 75–80.
94. Santner-Nanan, B., Straubinger, K., Hsu, P., Parnell, G., Tang, B., Xu, B., et al. Fetal-maternal alignment of regulatory T cells correlates with IL-10 and Bcl-2 upregulation in pregnancy. J Immunol 191 (2013), 145–153.
95. Abelius, M.S., Lempinen, E., Lindblad, K., Ernerudh, J., Berg, G., Matthiesen, L., et al. Th2-like chemokine levels are increased in allergic children and influenced by maternal immunity during pregnancy. Pediatr Allergy Immunol 25 (2014), 387–393.
96. Abelius, M.S., Janefjord, C., Ernerudh, J., Berg, G., Matthiesen, L., Duchen, K., et al. The placental immune milieu is characterized by a Th2- and anti-inflammatory transcription profile, regardless of maternal allergy, and associates with neonatal immunity. Am J Reprod Immunol 73 (2015), 445–459.
97. Sandberg, M., Frykman, A., Ernerudh, J., Berg, G., Matthiesen, L., Ekerfelt, C., et al. Cord blood cytokines and chemokines and development of allergic disease. Pediatr Allergy Immunol 20 (2009), 519–527.
98. Abelius, M.S., Ernerudh, J., Berg, G., Matthiesen, L., Nilsson, L.J., Jenmalm, M.C., High cord blood levels of the T-helper 2-associated chemokines CCL17 and CCL22 precede allergy development during the first 6 years of life. Pediatr Res 70 (2011), 495–500.
99. Prescott, S.L., Macaubas, C., Smallacombe, T., Holt, B.J., Sly, P.D., Holt, P.G., Development of allergen-specific T-cell memory in atopic and normal children. Lancet 353 (1999), 196–200.
100. Tulic, M.K., Hodder, M., Forsberg, A., McCarthy, S., Richman, T., D'Vaz, N., et al. Differences in innate immune function between allergic and nonallergic children: new insights into immune ontogeny. J Allergy Clin Immunol, 127, 2011 470–8.e1.
101. Böttcher, M.F., Jenmalm, M.C., Björkstén, B., Immune responses to birch in young children during their first 7 years of life. Clin Exp Allergy 32 (2002), 1690–1698.
102. Hansel, T.T., Johnston, S.L., Openshaw, P.J., Microbes and mucosal immune responses in asthma. Lancet 381 (2013), 861–873.
103. Schaub, B., Liu, J., Hoppler, S., Schleich, I., Huehn, J., Olek, S., et al. Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells. J Allergy Clin Immunol, 123, 2009 774–82.e5.
104. Vuillermin, P.J., Ponsonby, A.L., Saffery, R., Tang, M.L., Ellis, J.A., Sly, P., et al. Microbial exposure, interferon gamma gene demethylation in naive T-cells, and the risk of allergic disease. Allergy 64 (2009), 348–353.
105. Fagerås, M., Tomicic, S., Voor, T., Björkstén, B., Jenmalm, M.C., Slow salivary secretory IgA maturation may relate to low microbial pressure and allergic symptoms in sensitized children. Pediatr Res 70 (2011), 572–577.
106. Kukkonen, K., Kuitunen, M., Haahtela, T., Korpela, R., Poussa, T., Savilahti, E., High intestinal IgA associates with reduced risk of IgE-associated allergic diseases. Pediatr Allergy Immunol 21 (2010), 67–73.
107. Sandin, A., Björkstén, B., Böttcher, M.F., Englund, E., Jenmalm, M.C., Bråbäck, L., High salivary secretory IgA antibody levels are associated with less late-onset wheezing in IgE-sensitized infants. Pediatr Allergy Immunol 22 (2011), 477–481.
108. Forsberg, A., Abrahamsson, T.R., Björkstén, B., Jenmalm, M.C., Pre- and post-natal Lactobacillus reuteri supplementation decreases allergen responsiveness in infancy. Clin Exp Allergy 43 (2013), 434–442.
109. Prescott, S.L., Wickens, K., Westcott, L., Jung, W., Currie, H., Black, P.N., et al. Supplementation with Lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin A detection. Clin Exp Allergy 38 (2008), 1606–1614.
110. Kopp, M.V., Goldstein, M., Dietschek, A., Sofke, J., Heinzmann, A., Urbanek, R., Lactobacillus GG has in vitro effects on enhanced interleukin-10 and interferon-gamma release of mononuclear cells but no in vivo effects in supplemented mothers and their neonates. Clin Exp Allergy 38 (2008), 602–610.
111. Boyle, R.J., Mah, L.J., Chen, A., Kivivuori, S., Robins-Browne, R.M., Tang, M.L., Effects of Lactobacillus GG treatment during pregnancy on the development of fetal antigen-specific immune responses. Clin Exp Allergy 38 (2008), 1882–1890.
112. Ro, A.D.B., Simpson, M.R., Ro, T.B., Storro, O., Johnsen, R., Videm, V., et al. Reduced Th22 cell proportion and prevention of atopic dermatitis in infants following maternal probiotic supplementation. Clin Exp Allergy 47 (2017), 1014–1021.
113. Sonnenberg, G.F., Fouser, L.A., Artis, D., Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12 (2011), 383–390.
114. Gutzeit, C., Magri, G., Cerutti, A., Intestinal IgA production and its role in host-microbe interaction. Immunol Rev 260 (2014), 76–85.
115. Marschan, E., Kuitunen, M., Kukkonen, K., Poussa, T., Sarnesto, A., Haahtela, T., et al. Probiotics in infancy induce protective immune profiles that are characteristic for chronic low-grade inflammation. Clin Exp Allergy 38 (2008), 611–618.
116. Böttcher, M.F., Abrahamsson, T.R., Fredriksson, M., Jakobsson, T., Björkstén, B., Low breast milk TGF-beta2 is induced by Lactobacillus reuteri supplementation and associates with reduced risk of sensitization during infancy. Pediatr Allergy Immunol 19 (2008), 497–504.
117. Kuitunen, M., Kukkonen, A.K., Savilahti, E., Impact of maternal allergy and use of probiotics during pregnancy on breast milk cytokines and food antibodies and development of allergy in children until 5 years. Int Arch Allergy Immunol 159 (2012), 162–170.
118. Miyara, M., Yoshioka, Y., Kitoh, A., Shima, T., Wing, K., Niwa, A., et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 30 (2009), 899–911.
119. Mjösberg, J., Svensson, J., Johansson, E., Hellström, L., Casas, R., Jenmalm, M.C., et al. Systemic reduction of functionally suppressive CD4dimCD25highFoxp3+ Tregs in human second trimester pregnancy is induced by progesterone and 17beta-estradiol. J Immunol 183 (2009), 759–769.
120. Taylor, A.L., Hale, J., Hales, B.J., Dunstan, J.A., Thomas, W.R., Prescott, S.L., FOXP3 mRNA expression at 6 months of age is higher in infants who develop atopic dermatitis, but is not affected by giving probiotics from birth. Pediatr Allergy Immunol 18 (2007), 10–19.
121. Forsberg, A., Abrahamsson, T.R., Björkstén, B., Jenmalm, M.C., Pre- and postnatal administration of Lactobacillus reuteri decreases TLR2 responses in infants. Clin Transl Allergy, 4, 2014, 21.
122. Davis, E.C., Wang, M., Donovan, S.M., The role of early life nutrition in the establishment of gastrointestinal microbial composition and function. Gut Microbes 8 (2017), 143–171.
123. Goodrich, J.K., Di Rienzi, S.C., Poole, A.C., Koren, O., Walters, W.A., Caporaso, J.G., et al. Conducting a microbiome study. Cell 158 (2014), 250–262.
124. Simonyte Sjödin, K., Vidman, L., Rydén, P., West, C.E., Emerging evidence of the role of gut microbiota in the development of allergic diseases. Curr Opin Allergy Clin Immunol 16 (2016), 390–395.
125. Gueimonde, M., Sakata, S., Kalliomäki, M., Isolauri, E., Benno, Y., Salminen, S., Effect of maternal consumption of lactobacillus GG on transfer and establishment of fecal bifidobacterial microbiota in neonates. J Pediatr Gastroenterol Nutr 42 (2006), 166–170.
126. Lahtinen, S.J., Boyle, R.J., Kivivuori, S., Oppedisano, F., Smith, K.R., Robins-Browne, R., et al. Prenatal probiotic administration can influence Bifidobacterium microbiota development in infants at high risk of allergy. J Allergy Clin Immunol 123 (2009), 499–501.
127. Dotterud, C.K., Avershina, E., Sekelja, M., Simpson, M.R., Rudi, K., Storro, O., et al. Does maternal perinatal probiotic supplementation alter the intestinal microbiota of mother and child?. J Pediatr Gastroenterol Nutr 61 (2015), 200–207.
128. Rutten, N.B., Gorissen, D.M., Eck, A., Niers, L.E., Vlieger, A.M., Besseling-van der Vaart, I., et al. Long term development of gut microbiota composition in atopic children: impact of probiotics. PLoS One, 10, 2015, e0137681.
129. West, C.E., Gothefors, L., Granström, M., Käyhty, H., Hammarström, M.L., Hernell, O., Effects of feeding probiotics during weaning on infections and antibody responses to diphtheria, tetanus and Hib vaccines. Pediatr Allergy Immunol 19 (2008), 53–60.
130. Avershina, E., Cabrera Rubio, R., Lundgard, K., Perez Martinez, G., Collado, M.C., Storro, O., et al. Effect of probiotics in prevention of atopic dermatitis is dependent on the intrinsic microbiota at early infancy. J Allergy Clin Immunol, 139, 2017 1399–1402.e8.
131. Chorell, E., Karlsson Videhult, F., Hernell, O., Antti, H., West, C.E., Impact of probiotic feeding during weaning on the serum lipid profile and plasma metabolome in infants. Br J Nutr 110 (2013), 116–126.
132. Thomas, D.W., Greer, F.R., Probiotics and prebiotics in pediatrics. Pediatrics 126 (2010), 1217–1231.
133. Panel, N.I.-S.E., Boyce, J.A., Assa'ad, A., Burks, A.W., Jones, S.M., Sampson, H.A., et al. 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 (2010), S1–S58.
134. Muraro, A., Agache, I., Clark, A., Sheikh, A., Roberts, G., Akdis, C.A., et al. EAACI food allergy and anaphylaxis guidelines: managing patients with food allergy in the community. Allergy 69 (2014), 1046–1057.
135. Braegger, C., Chmielewska, A., Decsi, T., Kolacek, S., Mihatsch, W., Moreno, L., et al. Supplementation of infant formula with probiotics and/or prebiotics: a systematic review and comment by the ESPGHAN committee on nutrition. J Pediatr Gastroenterol Nutr 52 (2011), 238–250.
136. Morelli, L., Capurso, L., FAO/WHO guidelines on probiotics: 10 years later. J Clin Gastroenterol 46:Suppl (2012), S1–S2.
137. Fiocchi, A., Pawankar, R., Cuello-Garcia, C., Ahn, K., Al-Hammadi, S., Agarwal, A., et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): probiotics. World Allergy Organ J, 8, 2015, 4.
138. Dugoua, J.J., Machado, M., Zhu, X., Chen, X., Koren, G., Einarson, T.R., Probiotic safety in pregnancy: a systematic review and meta-analysis of randomized controlled trials of Lactobacillus, Bifidobacterium, and Saccharomyces spp. J Obstet Gynaecol Can 31 (2009), 542–552.
139. Karlsson Videhult, F., Öhlund, I., Stenlund, H., Hernell, O., West, C.E., Probiotics during weaning: a follow-up study on effects on body composition and metabolic markers at school age. Eur J Nutr 54 (2015), 355–363.
140. Karlsson Videhult, F., Andersson, Y., Öhlund, I., Stenlund, H., Hernell, O., West, C.E., Impact of probiotics during weaning on the metabolic and inflammatory profile: follow-up at school age. Int J Food Sci Nutr 66 (2015), 686–691.
141. West, C.E., Probiotics for allergy prevention. Benef Microbes 7 (2016), 171–179.