Microbial influence on tolerance and opportunities for intervention with prebiotics/probiotics and bacterial lysates

Journal of Allergy and Clinical Immunology

Volumn 131, Issue 6, 2013, Pages 1453-1463

  Pfefferle, Petra Ina ^a,b   Prescott, Susan L ^b,c   Kopp, Matthias ^d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY HOSPITAL MARBURG   (Germany)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSITY OF LÜBECK   (Germany)

Author keywords

allergic disease; allergy; bacterial lysates; Developmental Origins of Health and Disease; immune tolerance; Microbiome; prebiotics; prevention; probiotics

Indexed keywords

BACTERIUM LYSATE; CYTOKINE; FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; GAMMA INTERFERON; LW 50020; PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT; PROSYMBIOFLOR; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ALLERGIC DISEASE; ALLERGIC RHINITIS; ALLERGIC URTICARIA; ATOPIC DERMATITIS; ATOPY; BIFIDOBACTERIUM; BIFIDOBACTERIUM LONGUM; CELLULAR IMMUNITY; CHILD HEALTH CARE; CLINICAL TRIAL (TOPIC); COMMON COLD; ECZEMA; ENTERITIS; ENVIRONMENTAL FACTOR; FECES MICROFLORA; FETUS DEVELOPMENT; FOOD ALLERGY; GASTROINTESTINAL DISEASE; HAY FEVER; HOMEOSTASIS; HUMAN; IMMUNOLOGICAL TOLERANCE; INFLAMMATORY DISEASE; INNATE IMMUNITY; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE INFECTION; INTESTINE LYMPHATIC TISSUE; LACTOBACILLUS; LACTOBACILLUS PARACASEI; LACTOBACILLUS RHAMNOSUS; LIFESTYLE MODIFICATION; MICROBIAL COLONIZATION; NONHUMAN; OUTCOME ASSESSMENT; PERINATAL PERIOD; PREGNANCY; PRENATAL PERIOD; PRIMARY PREVENTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFECTION; REVIEW; RHINOCONJUNCTIVITIS; RISK FACTOR; SENSITIZATION; VAGINA FLORA; VIRAL RESPIRATORY TRACT INFECTION;

CHRONIC DISEASE; CLINICAL TRIALS AS TOPIC; FEMALE; HUMANS; HYPERSENSITIVITY; IMMUNE TOLERANCE; INFLAMMATION; MATERNAL EXPOSURE; PERINATAL CARE; PREBIOTICS; PROBIOTICS;

EID: 84878539490     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2013.03.020     Document Type: Review

References (98)

1. M.V. Thrusfield Veterinary epidemiology 2nd ed. 1985 Blackwell Science Oxford (United Kingdom)
2. A. Gonzalez, J.C. Clemente, A. Shade, J.L. Metcalf, S. Song, and B. Prithiviraj Our microbial selves: what ecology can teach us EMBO Rep 12 2011 775 784
3. C. Stephens Microbiology: intimate strangers Curr Biol 10 2000 R272 R275
4. L.K. Ursell, J.C. Clemente, J.R. Rideout, D. Gevers, J.G. Caporaso, and R. Knight The interpersonal and intrapersonal diversity of human-associated microbiota in key body sites J Allergy Clin Immunol 129 2012 1204 1208
5. B.P. Willing, L.C. Antunes, K.M. Keeney, R.B. Ferreira, and B.B. Finlay Harvesting the biological potential of the human gut microbiome Bioessays 33 2011 414 418
6. I. Jarchum, and E.G. Pamer Regulation of innate and adaptive immunity by the commensal microbiota Curr Opin Immunol 23 2011 353 360
7. E. von Mutius 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: farm lifestyles and the hygiene hypothesis Clin Exp Immunol 160 2010 130 135
8. L. von Hertzen, and I. Hanski Haahtela T Natural immunity. Biodiversity loss and inflammatory diseases are two global megatrends that might be related EMBO Rep 12 2011 1089 1093
9. J. Schrezenmeir, and M. de Vrese Probiotics, prebiotics, and synbiotics - approaching a definition Am J Clin Nutr 73 suppl 2001 361S 364S
10. E. Metchnikoff The prolongation of life. Optimistic studies 1907 Butterworth-Heinemann London
11. A. Nissle Die antagonistische Behandlung chronischer Darmstörungen mit Colibakterien Med Klin 2 1918 29 33
12. R.M. McLoughlin, and K.H. Mills Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma J Allergy Clin Immunol 127 2011 1097 1109
13. L. Hatzler, S. Hofmaier, and N.G. Papadopoulos Allergic airway diseases in childhood - marching from epidemiology to novel concepts of prevention Pediatr Allergy Immunol 23 2012 616 622
14. G. Lack Update on risk factors for food allergy J Allergy Clin Immunol 129 2012 1187 1197
15. N. Blumer, U. Herz, M. Wegmann, and H. Renz Prenatal lipopolysaccharide- exposure prevents allergic sensitisation and airway inflammation, but not airway responsiveness in a murine model of experimental asthma Clin Exp Allergy 35 2005 397 402
16. N. Blumer, S. Sel, S. Virna, C.C. Patrascan, S. Zimmermann, and U. Herz Perinatal maternal application of Lactobacillus rhamnosus GG suppresses allergic airway inflammation in mouse offspring Clin Exp Allergy 37 2007 348 357
17. C. Braun-Fahrlander, J. Riedler, U. Herz, W. Eder, M. Waser, and L. Grize Environmental exposure to endotoxin and its relation to asthma in school-age children N Engl J Med 347 2002 869 877
18. M.J. Ege, C. Bieli, R. Frei, R.T. van Strien, J. Riedler, and E. Ublagger Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children J Allergy Clin Immunol 117 2006 817 823
19. B. Schaub, J. Liu, S. Hoppler, I. Schleich, J. Huehn, and S. Olek Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells J Allergy Clin Immunol 123 2009 774 782.e5
20. S. Brand, R. Teich, T. Dicke, H. Harb, A.O. Yildirim, and J. Tost Epigenetic regulation of in murine offspring as a novel mechanism for transmaternal asthma protection induced by microbes J Allergy Clin Immunol 128 2011 618 625
21. M.L. Conrad, R. Ferstl, R. Teich, S. Brand, N. Blumer, and A.O. Yildirim Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78 J Exp Med 206 2009 2869 2877
22. S.L. Prescott, M. Tulic, A. Osei-Kumah, T. Richman, M. Crook, and D. Martino Reduced placental FOXP3 associated with subsequent infant allergic disease J Allergy Clin Immunol 128 2011 886 887.e5
23. M. Tulic, A. Forsberg, M. Hodder, S. McCarthy, D. Martino, and N. de Vaz Differences in the developmental trajectory of innate microbial responses in atopic and normal children: new insights into immune ontogeny J Allergy Clin Immunol 127 2011 470 478
24. S. Prescott, C. Macaubas, B. Holt, T. Smallacombe, R. Loh, and P. Sly Transplacental priming of the human immune system to environmental allergens: universal skewing of initial T-cell responses towards Th-2 cytokine profile J Immunol 160 1998 4730 4737
25. J.G. Lisciandro, S.L. Prescott, M.G. Nadal-Sims, C.J. Devitt, P.C. Richmond, and W. Pomat Neonatal antigen-presenting cells are functionally more quiescent in children born under traditional compared with modern environmental conditions J Allergy Clin Immunol 130 2012 1167 1174.e10
26. J.G. Lisciandro, S.L. Prescott, M.G. Nadal-Sims, C.J. Devitt, W. Pomat, and P.M. Siba Comparison of neonatal T regulatory cell function in Papua New Guinean and Australian newborns Pediatr Allergy Immunol 23 2012 173 180
27. S.L. Prescott, K. Wickens, L. Westcott, W. Jung, H. Currie, and P.N. Black 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
28. R.J. Boyle, L.J. Mah, A. Chen, S. Kivivuori, R.M. Robins-Browne, and M.L. Tang Effects of Lactobacillus GG treatment during pregnancy on the development of fetal antigen-specific immune responses Clin Exp Allergy 38 2008 1882 1890
29. K. Wickens, P.N. Black, T.V. Stanley, E. Mitchell, P. Fitzharris, and G.W. Tannock 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
30. M. Kalliomaki, S. Salminen, H. Arvilommi, P. Kero, P. Koskinen, and E. Isolauri Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial Lancet 357 2001 1076 1079
31. M.V. Kopp, I. Hennemuth, A. Dietschek, M. Goldstein, G. Ihorst, and A. Heinzmann A randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical or immunological effects of Lactobacillus GG supplementation Pediatrics 121 2008 e850 e856
32. A. Huurre, K. Laitinen, S. Rautava, M. Korkeamäki, and E. Isolauri 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
33. K. Kukkonen, E. Savilahti, T. Haahtela, K. Juntunen-Backman, R. Korpela, and T. Poussa 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
34. S.E. Soh, M. Aw, I. Gerez, Y.S. Chong, M. Rauff, and Y.P. Ng 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
35. T.R. Abrahamsson, T. Jakobsson, M.F. Bottcher, M. Fredrikson, M.C. Jenmalm, and B. Bjorksten Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial J Allergy Clin Immunol 119 2007 1174 1180
36. C.K. Dotterud, O. Storrø, R. Johnsen, and T. Oien Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial Br J Dermatol 163 2010 616 623
37. J.Y. Kim, J.H. Kwon, S.H. Ahn, S.I. Lee, Y.S. Han, and Y.O. Choi 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
38. L. Niers, R. Martín, G. Rijkers, F. Sengers, H. Timmerman, and N. van Uden The effects of selected probiotic strains on the development of eczema (the PandA study) Allergy 64 2009 1349 1358
39. A.L. Taylor, J.A. Dunstan, and S.L. Prescott 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
40. C. Grüber, M. van Stuijvenberg, F. Mosca, G. Moro, G. Chirico, and C.P. Braegger Reduced occurrence of early atopic dermatitis because of immunoactive prebiotics among low-atopy-risk infants J Allergy Clin Immunol 126 2010 791 797
41. R.J. Boyle, I.H. Ismail, S. Kivivuori, P.V. Licciardi, R.M. Robins-Browne, and L.J. Mah Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial Allergy 66 2011 509 516
42. S. Rautava, E. Kainonen, S. Salminen, and E. Isolauri Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant J Allergy Clin Immunol 130 2012 1355 1360
43. M. Kalliomaki, S. Salminen, T. Poussa, and E. Isolauri 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
44. M. Kalliomaki, S. Salminen, T. Poussa, H. Arvilommi, and E. Isolauri Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial Lancet 361 2003 1869 1871
45. M. Kuitunen, K. Kukkonen, K. Juntunen-Backman, R. Korpela, T. Poussa, and T. Tuure 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
46. S. Rautava, H. Arvilommi, and E. Isolauri Specific probiotics in enhancing maturation of IgA responses in formula-fed infants Pediatr Res 60 2006 221 224
47. C.E. West, M.L. Hammarström, and O. Hernell Probiotics during weaning reduce the incidence of eczema Pediatr Allergy Immunol 20 2009 430 437
48. R. Lodinová-Zádníková, L. Prokesová, I. Kocourková, J. Hrdý, and J. Zizka Prevention of allergy in infants of allergic mothers by probiotic Escherichia coli Int Arch Allergy Immunol 153 2010 201 206
49. M.A. Rose, F. Stieglitz, A. Köksal, R. Schubert, J. Schulze, and S. Zielen Efficacy of probiotic Lactobacillus GG on allergic sensitization and asthma in infants at risk Clin Exp Allergy 40 2010 1398 1405
50. K. Wickens, P. Black, T.V. Stanley, E. Mitchell, C. Barthow, and P. Fitzharris 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 2012 1071
51. M.L. Tang, S.J. Lahtinen, and R.J. Boyle Probiotics and prebiotics: clinical effects in allergic disease Curr Opin Pediatr 22 2010 626 634
52. D.A. Osborn, and J.K. Sinn Prebiotics in infants for prevention of allergic disease and food hypersensitivity Cochrane Database Syst Rev 4 2007 CD006474
53. J. Lee, D. Seto, and L. Bielory Meta-analysis of clinical trials of probiotics for prevention and treatment of pediatric atopic dermatitis J Allergy Clin Immunol 121 2008 116 121.e11
54. K. Doege, D. Grajecki, B.C. Zyriax, E. Detinkina, C. Zu Eulenburg, and K.J. Buhling Impact of maternal supplementation with probiotics during pregnancy on atopic eczema in childhood - a meta-analysis Br J Nutr 107 2012 1 6
55. C. Pelucchi, L. Chatenoud, F. Turati, C. Galeone, L. Moja, and J.F. Bach Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis Epidemiology 23 2012 402 414
56. R. Fujiwara, N. Takemura, J. Watanabe, and K. Sonoyama Maternal consumption of fructo-oligosaccharide diminishes the severity of skin inflammation in offspring of NC/Nga mice Br J Nutr 103 2010 530 538
57. A.D. Maurer, and R.A. Reimer Maternal consumption of high-prebiotic fibre or -protein diets during pregnancy and lactation differentially influences satiety hormones and expression of genes involved in glucose and lipid metabolism in offspring in rats Br J Nutr 105 2011 329 338
58. G. Moro, S. Arslanoglu, B. Stahl, J. Jelinek, U. Wahn, and G. Boehm A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age Arch Dis Child 91 2006 814 819
59. S. Arslanoglu, G.E. Moro, J. Schmitt, L. Tandoi, S. Rizzardi, and G. Boehm Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life J Nutr 138 2008 1091 1095
60. C.Y. Ou, H.C. Kuo, L. Wang, T.Y. Hsu, H. Chuang, and C.A. Liu 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
61. A.C. Ouwehand, E. Isolauri, P.V. Kirjavainen, S. Tölkko, and S.J. Salminen The mucus binding of Bifidobacterium lactis Bb12 is enhanced in the presence of Lactobacillus GG and Lact. delbrueckii subsp. bulgaricus Lett Appl Microbiol 30 2000 10 13
62. Ł. Grześkowiak, M.M. Grönlund, C. Beckmann, S. Salminen, A. von Berg, and E. Isolauri The impact of perinatal probiotic intervention on gut microbiota: double-blind placebo-controlled trials in Finland and Germany Anaerobe 18 2012 7 13
63. M. Cazzola, P. Rogliani, and G. Curradi Bacterial extracts for the prevention of acute exacerbations in chronic obstructive pulmonary disease: a point of view Respir Med 102 2008 321.e7
64. A. Roży, and J. Chorostowska-Wynimko Bacterial immunostimulants - mechanism of action and clinical application in respiratory diseases Pneumonol Alergol Pol 76 2008 353 359
65. J.M. Puigdollers, G.R. Serna, I. Hernandez del Rey, M.T. Barruffet, and J.J. Torroella Immunoglobulin production in man stimulated by an orally administered bacterial lysate Respiration 40 1980 142 149
66. G.A. Rossi, C. Peri, M.E. Raynal, A.C. Defilippi, F.M. Risso, and G. Schenone Naturally occurring immune response against bacteria commonly involved in upper respiratory tract infections: analysis of the antigen-specific salivary IgA levels Immunol Lett 86 2003 85 91
67. M. Huber, H. Mossmann, and W.G. Bessler Th1-orientated immunological properties of the bacterial extract OM-85-BV Eur J Med Res 10 2005 209 217
68. T. Rogosch, S. Kerzel, K. Hoß, G. Hoersch, C. Zemlin, and M. Heckmann IgA response in preterm neonates shows little evidence of antigen-driven selection J Immunol 189 2012 5449 5456
69. M. Cazzola, A. Capuano, P. Rogliani, and M.G. Matera Bacterial lysates as a potentially effective approach in preventing acute exacerbation of COPD Curr Opin Pharmacol 12 2012 300 308
70. M. Weinberger Can we prevent exacerbations of asthma caused by common cold viruses? J Allergy Clin Immunol 126 2010 770 771
71. C.H. Razi, K. Harmanci, A. Abaci, O. Özdemir, S. Hizli, and R. Renda The immunostimulant OM-85 BV prevents wheezing attacks in preschool children J Allergy Clin Immunol 126 2010 763 769
72. L.M. Bowman, and P.G. Holt Selective enhancement of systemic Th1 immunity in immunologically immature rats with an orally administered bacterial extract Infect Immun 69 2001 3719 3727
73. D.H. Strickland, S. Judd, J.A. Thomas, A.N. Larcombe, P.D. Sly, and P.G. Holt Boosting airway T-regulatory cells by gastrointestinal stimulation as a strategy for asthma control Mucosal Immunol 4 2011 43 52
74. S. Navarro, G. Cossalter, C. Chiavaroli, A. Kanda, S. Fleury, and A. Lazzari The oral administration of bacterial extracts prevents asthma via the recruitment of regulatory T cells to the airway Mucosal Immunol 4 2011 53 65
75. C. Steurer-Stey, L. Lagler, D.A. Straub, J. Steurer, and L.M. Bachmann Oral purified bacterial extracts in acute respiratory tract infections in childhood: a systematic quantitative review Eur J Pediatr 166 2007 365 376
76. U.B. Schaad OM-85 BV, an immunostimulant in pediatric recurrent respiratory tract infections: a systematic review World J Pediatr 6 2010 5 12
77. M. Cazzola, S. Anapurapu, and C.P. Page Polyvalent mechanical bacterial lysate for the prevention of recurrent respiratory infections: a meta-analysis Pulm Pharmacol Ther 25 2012 62 68
78. C. Ruedl, M. Frühwirth, G. Wick, and H. Wolf Immune response in the lungs following oral immunization with bacterial lysates of respiratory pathogens Clin Diagn Lab Immunol 1 1994 150 154
79. G.C. Faure, M.C. Bene, C. Simon, and A. Quantain Increase in specific antibody-forming cells in human tonsils after oral stimulation with D-53, a ribosomal vaccine Int J Immunopharmacol 12 1990 315 320
80. W. Jongmans, D.M. Tiemessen, I.J. van Vlodrop, P.F. Mulders, and E. Oosterwijk Th1-polarizing capacity of clinical-grade dendritic cells is triggered by Ribomunyl but is compromised by PGE2: the importance of maturation cocktails J Immunother 28 2005 480 487
81. M. Rutishauser, P. Pitzke, G. Grevers, A. van Aubel, U. Elsasser, and A. Kämmereit Use of a polyvalent bacterial lysate in patients with recurrent respiratory tract infections: results of a prospective, placebo-controlled, randomized, double-blind study Adv Ther 15 1998 330 341
82. S.B. Ruah, C. Ruah, A. van Aubel, S. Abel, and U. Elsasser Efficacy of a polyvalent bacterial lysate in children with recurrent respiratory tract infections Adv Ther 18 2001 151 162
83. P. Boyle, J.A. Bellanti, and C. Robertson Meta-analysis of published clinical trials of a ribosomal vaccine (ribomunyl) in prevention of respiratory infections BioDrugs 14 2000 389 408
84. L. Brunetti, R. Francavilla, R. Tesse, P. Fiermonte, P. Dambra, and M. Massagli Effects of oral bacterial immunotherapy in children with atopic eczema/dermatitis syndrome: a pilot study BioDrugs 19 2005 393 399
85. W.K. Podleski Immunomodulation of allergic autocytotoxicity in bronchial asthma by a bacterial lysate - Broncho-Vaxom Int J Immunopharmacol 7 1985 713 718
86. J. Riedler, C. Braun-Fahrländer, W. Eder, M. Schreuer, M. Waser, and S. Maisch Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey Lancet 358 2001 1129 1133
87. S. Lau, K. Gerhold, K. Zimmermann, C.W. Ockeloen, S. Rossberg, and P. Wagner Oral application of bacterial lysate in infancy decreases the risk of atopic dermatitis in children with 1 atopic parent in a randomized, placebo-controlled trial J Allergy Clin Immunol 129 2012 1040 1047
88. A.R. Jadad, R.A. Moore, D. Carroll, C. Jenkinson, D.J. Reynolds, and D.J. Gavaghan Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17 1996 1 12
89. N. Sudo, S. Sawamura, K. Tanaka, Y. Aiba, C. Kubo, and Y. Koga The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction J Immunol 159 1997 1739 1745
90. B.P. Boerner, and N.E. Sarvetnick Type 1 diabetes: role of intestinal microbiome in humans and mice Ann N Y Acad Sci 1243 2011 103 118
91. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, and J.I. Gordon An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 2006 1027 1031
92. P. Bercik, E. Denou, J. Collins, W. Jackson, J. Lu, and J. Jury The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice Gastroenterology 141 2011 599 609 e1-3
93. T.R. Abrahamsson, H.E. Jakobsson, A.F. Andersson, B. Bjorksten, L. Engstrand, and M.C. Jenmalm Low diversity of the gut microbiota in infants with atopic eczema J Allergy Clin Immunol 129 2012 434 440 e1-2
94. F.A. van Nimwegen, J. Penders, E.E. Stobberingh, D.S. Postma, G.H. Koppelman, and M. Kerkhof Mode and place of delivery, gastrointestinal microbiota, and their influence on asthma and atopy J Allergy Clin Immunol 128 2011 948 955 e1-3
95. H. Bisgaard, N. Li, K. Bonnelykke, B.L. Chawes, T. Skov, and G. Paludan-Muller 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 646 652 e1-5
96. P. Bercik, S.M. Collins, and E.F. Verdu Microbes and the gut-brain axis Neurogastroenterol Motil 24 2012 405 413
97. P.J. Turnbaugh, F. Backhed, L. Fulton, and J.I. Gordon Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome Cell Host Microbe 3 2008 213 223
98. J.K. Harris, and B.D. Wagner Bacterial identification and analytic challenges in clinical microbiome studies J Allergy Clin Immunol 129 2012 441 442