External influence of early childhood establishment of gut microbiota and subsequent health implications

Frontiers in Pediatrics

Volumn 2, Issue OCT, 2014, Pages

  Munyaka, Peris Mumbi ^a   Khafipour, Ehsan ^a   Ghia, Jean Eric ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Antibiotics; Cesarean section; Diet; Gut microbiota; Immunity; Inflammatory diseases

Indexed keywords

EID: 85050920580     PISSN: None     EISSN: 22962360     Source Type: Journal    
DOI: 10.3389/fped.2014.00109     Document Type: Review

References (102)

1. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature (2010) 464:59-65. doi:10.1038/nature08821
2. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell (2006) 124:837-48. doi:10.1016/j.cell.2006.02.017
3. Bjorksten B. Diverse microbial exposure-consequences for vaccine development. Vaccine (2012) 30:4336-40. doi:10.1016/j.vaccine.2011.10.074
4. Young VB. The intestinal microbiota in health and disease. Curr Opin Gastroenterol (2012) 28:63-9. doi:10.1097/MOG.0b013e32834d61e9
5. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature (2012) 489:231-41. doi:10.1038/nature11551
6. Li M, Wang M, Donovan SM. Early development of the gut microbiome and immune-mediated child disorders. Semin Reprod Med (2014) 32:74-86. doi:10.1055/s-0033-1361825
7. Kozyrskyj AL, Bahreinian S, Azad MB. Early life exposures: impact on asthma and allergic disease. Curr Opin Allergy Clin Immunol (2011) 11:400-6. doi:10.1097/ACI.0b013e328349b166
8. Human Microbiome Project C. A framework for human microbiome research. Nature (2012) 486:215-21. doi:10.1038/nature11209
9. Suau A, Bonnet R, Sutren M, Gordon JJ, Gibson GR, Collins MD, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol (1999) 65:4799-807
10. Gerber GK. The dynamic microbiome. FEBS Lett (2014). doi:10.1016/j.febslet.2014.02.037
11. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett C, Knight R, Gordon JI. The human microbiome project. Nature (2007) 449:804-10. doi:10.1038/nature06244
12. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende D, et al. Enterotypes of the human gut microbiome. Nature (2011) 473:174-80. doi:10.1038/nature09944
13. Vanhoutte T, Huys G, Brandt E, Swings J. Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol Ecol (2004) 48:437-46. doi:10.1016/j.femsec.2004.03.001
14. De La Cochetiere MF, Durand T, Lepage P, Bourreille A, Galmiche JP, Dore J. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol (2005) 43:5588-92. doi:10.1128/JCM.43.11.5588-5592.2005
15. Rook GA, Lowry CA, Raison CL. Hygiene and other early childhood influences on the subsequent function of the immune system. Brain Res (2014). doi:10.1016/j.brainres.2014.04.004
16. Penders J, Kummeling I, Thijs C. Infant antibiotic use and wheeze and asthma risk: a systematic review and meta-analysis. Eur Respir J (2011) 38:295-302. doi:10.1183/09031936.00105010
17. Thavagnaman S, Fleming J, Bromley A, Shields MD, Cardwell CR. A meta-analysis of the association between caesarean section and childhood asthma. Clin Exp Allergy (2008) 38:629-33. doi:10.1111/j.1365-2222.2007.02780.x
18. Jimenez E, Marin ML, Martin R, Odriozola JM, Olivares M, Xaus J, et al. Is meconium from healthy newborns actually sterile? Res Microbiol (2008) 159:187-93. doi:10.1016/j.resmic.2007.12.007
19. Jimenez E, Fernandez L, Marin M, Martin R, Odriozola JM, Nueno-Palop C, et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol (2005) 51:270-4. doi:10.1007/s00284-005-0020-3
20. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One (2008) 3:e3056. doi:10.1371/journal.pone.0003056
21. Penders J, Thijs C, Vink C, Stelma FF, Kummeling IS, Van den Brandt PA, et al. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics (2006) 118:511-21. doi:10.1542/peds.2005-2824
22. Mackie RI, Sghir A, Gaskins HR. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr (1999) 69:S1035-45
23. Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E. Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol (2009) 48:8-12. doi:10.1111/j.1472-765X.2008.02475.x
24. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med (2014) 6:237ra65. doi:10.1126/scitranslmed.3008599
25. Madan JC, Salari RC, Saxena D, Davidson L, O'Toole GA, Moore JH, et al. Gut microbial colonisation in premature neonates predicts neonatal sepsis. Arch Dis Child Fetal Neonatal Ed (2012) 97:F456-62. doi:10.1136/fetalneonatal-2011-301373
26. Bailey MT, Lubach GR, Coe CL. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr (2004) 38:414-21. doi:10.1097/00005176-200404000-00009
27. Lahtinen SJ, Boyle RJ, Kivivuori S, Oppedisano F, Smith KR, Robins-Browne R, et al. Prenatal probiotic administration can influence Bifidobacterium microbiota development in infants at high risk of allergy. J Allergy Clin Immunol (2009) 123:499-501. doi:10.1016/j.jaci.2008.11.034
28. Faa G, Gerosa C, Fanni D, Nemolato S, van Eyken P, Fanos V. Factors influencing the development of a personal tailored microbiota in the neonate, with particular emphasis on antibiotic therapy. J Matern Fetal Neonatal Med (2013) 26(S2):35-43. doi:10.3109/14767058.2013.829700
29. Westerbeek EA, van den Berg A, Lafeber HN, Knol J, Fetter WP, van Elburg RM. The intestinal bacterial colonization in preterm infants: a review of the literature. Clin Nutr (2006) 25:361-8. doi:10.1016/j.clnu.2006.03.002
30. Droste JH, Wieringa MH, Weyler JJ, Nelen VJ, Vermeire PA, Van Bever HP. Does the use of antibiotics in early childhood increase the risk of asthma and allergic disease? Clin Exp Allergy (2000) 30:1548-53. doi:10.1046/j.1365-2222.2000.00939.x
31. Metsala J, Lundqvist A, Virta LJ, Kaila M, Gissler M, Virtanen SM. Mother's and offspring's use of antibiotics and infant allergy to cow's milk. Epidemiology (2013) 24:303-9. doi:10.1097/EDE.0b013e31827f520f
32. Russell SL, Gold MJ, Hartmann M, Willing BP, Thoson L, Wlodarska M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep (2012) 13:440-7. doi:10.1038/embor.2012.32
33. Stensballe LG, Simonsen J, Jensen SM, Bonnelykke K, Bisgaard H. Use of antibiotics during pregnancy increases the risk of asthma in early childhood. J Pediatr (2013) 162:832-8. doi:10.1016/j.jpeds.2012.09.049
34. Villarreal AA, Aberger FJ, Benrud R, Gundrum JD. Use of broad-spectrum antibiotics and the development of irritable bowel syndrome. WMJ (2012) 111:17-20
35. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol (2010) 105:2687-92. doi:10.1038/ajg.2010.398
36. Roberts SE, Wotton CJ, Williams JG, Griffith M, Goldacre MJ. Perinatal and early life risk factors for inflammatory bowel disease. World J Gastroenterol (2011) 17:743-9. doi:10.3748/wjg.v17.i6.743
37. Hviid A, Svanstrom H, Frisch M. Antibiotic use and inflammatory bowel diseases in childhood. Gut (2011) 60:49-54. doi:10.1136/gut.2010.219683
38. Biedermann L, Zeitz J, Mwinyi J, Sutter-Minder E, Rehman A, Ott SJ, et al. Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS One (2013) 8:e59260. doi:10.1371/journal.pone.0059260
39. Sakata H, Yoshioka H, Fujita K. Development of the intestinal flora in very low birth weight infants compared to normal full-term newborns. Eur J Pediatr (1985) 144:186-90. doi:10.1007/BF00451911
40. Gewolb IH, Schwalbe RS, Taciak VL, Harrison TS, Panigrahi P. Stool microflora in extremely low birthweight infants. Arch Dis Child Fetal Neonatal Ed (1999) 80:F167-73. doi:10.1136/fn.80.3.F167
41. Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, et al. Conditions of Bifidobacterial colonization in preterm infants: a prospective analysis. J Pediatr Gastroenterol Nutr (2007) 44:577-82. doi:10.1097/MPG.0b013e3180406b20
42. Azad MB, Konya T, Maughan H, Guttman DS, Field CJ, Chari RS, et al. Gut microbiota of healthy Canadian infants: profiles by mode of delivery and infant diet at 4 months. CMAJ (2013) 185:385-94. doi:10.1503/cmaj.121189
43. Matamoro S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere MF. Development of intestinal microbiota in infants and its impact on health. Trends Microbiol (2013) 21:167-73. doi:10.1016/j.tim.2012.12.001
44. Biasucci G, Benenati B, Morelli L, Bessi E, Boehm G. Cesarean delivery may affect the early biodiversity of intestinal bacteria. J Nutr (2008) 138:1796S-800S
45. Neu J, Rushing J. Caesarean versus vaginal delivery: long term infant outcomes and the hygiene hypothesis. Clin Perinatol (2011) 38:321-31. doi:10.1016/j.clp.2011.03.008
46. Jakobsson HE, Abrahamsson TR, Jenmalm MC, Harris K, Quince C, Jernberg C, et al. Decreased gut microbiota diversity, delayed Bacteroidetes colonization and reduced Th1 responses in infants delivered by caesarean section. Gut (2014) 63:559-66. doi:10.1136/gutjnl-2012-303249
47. Penders J, Gerhold K, Stobberingh EE, 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 (2013) 132:601-7. doi:10.1016/j.jaci.2013.05.043
48. Khafipour E, Ghia JE. Mode of delivery and inflammatory disorders. J Immunol Clin Res (2013) 1:1004
49. Dominguez-Bello MG, Blaser MJ, Ley RE, Knight R. Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology (2011) 140:1713-9. doi:10.1053/j.gastro.2011.02.011
50. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A (2010) 107:11971-5. doi:10.1073/pnas.1002601107
51. Cardwell CR, Stene LC, Joner G, Cinek O, Syenson J, Goldacre MJ, et al. Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia (2008) 51:726-35. doi:10.1007/s00125-008-0941-z
52. Valles Y, Artacho A, Pascual-Garcia A, Ferrus ML, Gosalbes MJ, Abellan JJ. Microbial succession in the gut: directional trends of taxonomic and functional change in a birth cohort of Spanish infants. PLoS Genet (2014) 10:e1004406. doi:10.1371/journal.pgen.1004406
53. Koening JE, Spor A, Scalfone NA, Stombaugh J, Knight R, Angenent LT, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A (2011) 108:4578-85. doi:10.1073/pnas.1000081107
54. Stark PL, Lee A. The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year. J Med Microbiol (1982) 15:189-203. doi:10.1099/00222615-15-2-189
55. Kramer MS. Breastfeeding and allergy: the evidence. Ann Nutr Metab (2011) 59(Suppl 1):20-6. doi:10.1159/000334148
56. Donnet-Hughes A, Perez PF, Dore J, Leclerc M, Levenez F, Benyacoub J, et al. Potential role of the intestinal microbiota of the mother in neonatal immune education. Proc Nutr Soc (2010) 69:407-15. doi:10.1017/S0029665110001898
57. Hunt KM, Foster JA, Formey LJ, Schutte UM, Beck DL, Abdo Z, et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS One (2011) 6:e21313. doi:10.1371/journal.pone.0021313
58. Jost T, Lacroix C, Braegger C, Chassard C. Assessment of bacterial diversity in breast milk using culture-dependent and culture-independent approaches. Br J Nutr (2013) 110:1253-62. doi:10.1017/S0007114513000597
59. Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother-neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol (2013) 3(3):203-20. doi:10.1111/1462-2920.12238
60. Garrido D, Barile D, Mills DA. A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract. Adv Nutr (2012) 3:415S-21S. doi:10.3945/an.111.001586
61. Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Nat Acad Sci U S A (2011) 108:4653-8. doi:10.1073/pnas.1000083107
62. Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut (2007) 56:661-7. doi:10.1136/gut.2006.100164
63. Bezirtzoglou E, Tsiotslas A, Weilling GW. Microbiota profile in feces of breast-and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe (2011) 17(6):478-82. doi:10.1016/j.anaerobe.2011.03.009
64. De Filippo C, Cavalieri D, Di Paola M, Ramazzoti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Nat Acad Sci U S A (2010) 107:14691-6. doi:10.1073/pnas.1005963107
65. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature (2012) 486:222-7. doi:10.1038/nature11053
66. Mulder IE, Schmidt B, Stokes CR, Lewis M, Bailey M, Aminoy RI, et al. Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biol (2009) 7:79. doi:10.1186/1741-7007-7-79
67. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol (2010) 2:53-66. doi:10.1093/gbe/evp057
68. Gronlund MM, Grzeskowiak L, Isolauri E, Salminen S. Influence of mother's intestinal microbiota on gut colonization in the infant. Gut Microbes (2011) 2:227-33. doi:10.4161/gmic.2.4.16799
69. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med (2011) 364:701-9. doi:10.1056/NEJMoa1007302
70. Sjögren YM, Jenmalm MC, Böttcher MF, Björkstén B, Sverremark-Ekström E. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin Exp Allergy (2009) 39:518-26. doi:10.1111/j.1365-2222.2008.03156.x
71. 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 (2012) 109:8334-9. doi:10.1073/pnas.1205624109
72. SherriffAJ. Hygiene levels in a contemporary population cohort are associated with wheezing and atopic eczema in preschool infants. Arch Dis Child (2002) 87:26-9. doi:10.1136/adc.87.1.26
73. Hesselmar B, Sjöberg F, Saalman R, Åberg N, Adlerberth I, Wold AE. Pacifier cleaning practices and risk of allergy development. Pediatrics (2013) 131:e1829-37. doi:10.1542/peds.2012-3345
74. Von Mutius E. Allergies, infections and the hygiene hypothesis-the epidemiological evidence. Immunobiology (2007) 212:433-9. doi:10.1016/j.imbio.2007.03.002
75. Benn CS, Melbye M, Wohlfahrt J, Björkstén B, Aaby P. Cohort study of sibling effect, infectious diseases, and risk of atopic dermatitis during first 18 months of life. Br Med J (2004) 328:1223-30. doi:10.1136/bmj.38069.512245.FE
76. Björkstén B. The hygiene hypothesis: do we still believe in it? Nestle Nutr Workshop Ser Pediatr Program (2009) 64:11-22; discussion 18-22. doi:10.1159/000235780
77. Kondrashova A, Hyoty H. Role of viruses and other microbes in the pathogenesis of type 1 diabetes. Int Rev Immunol (2014) 33(4):284-95. doi:10.3109/08830185.2014.889130
78. Hwang JS, Im CR, Im SH. Immune disorders and its correlation with gut microbiome. Immune Netw (2012) 12:129-38. doi:10.4110/in.2012.12.4.129
79. Lundell AC, Björnsson V, Ljung A, Ceder M, Johansen S, Lindhagen G, et al. Infant B cell memory differentiation and early gut bacterial colonization. J Immunol (2012) 188:4315-22. doi:10.4049/jimmunol.1103223
80. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med (2002) 347:911-20. doi:10.1056/NEJMra020100
81. Bisgaard H, Li N, Bonnelykke K, Chawes BL, 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 (2011) 128:646-52. doi:10.1016/j.jaci.2011.04.060
82. Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol (2012) 129:434-40. doi:10.1016/j.jaci.2011.10.025
83. Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy (2014) 44:842-50. doi:10.1111/cea.12253
84. Joffe TH, Simpson NA. Cesarean section and risk of asthma. The role of intra-partum antibiotics: a missing piece? J Pediatr (2009) 154:154. doi:10.1016/j.jpeds.2008.08.039
85. Johnson CC, Ownby DR, Alford SH, Havstad SL, Williams L, Zoratti EM, et al. Antibiotic exposure in early infancy and risk for childhood atopy. J Allergy Clin Immunol (2005) 115:1218-24. doi:10.1016/j.jaci.2005.04.020
86. Carlisle EM, Morowitz MJ. The intestinal microbiome and necrotizing enterocolitis. Curr Opin Pediatr (2013) 25:382-7. doi:10.1097/MOP.0b013e3283600e91
87. Torraza RM, Neu J. The altered gut microbiome and necrotizing enterocolitis. Clin Perinatol (2013) 40:93-108. doi:10.1016/j.clp.2012.12.009
88. Hällström M, Eerola E, Vuento R, Janas M, Tammela O. Effects of mode of delivery and necrotising enterocolitis on the intestinal microflora in preterm infants. Eur J Clin Microbiol Infect Dis (2004) 23:463-70. doi:10.1007/s10096-004-1146-0
89. Strachan D. Hay fever, hygiene and household size. Br Med J (1989) 299:1259-66. doi:10.1136/bmj.299.6710.1259
90. Ownby DR, Johnson CC, Peterson EL. Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA (2002) 288:963-72. doi:10.1001/jama.288.8.963
91. Fujimura KE, Demoor T, Rauch M, Faruqi AA, Jang S, Johnson CC, et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci U S A (2014) 111:805-10. doi:10.1073/pnas.1310750111
92. Forno E, Onderdonk AB, McCracken J, Litonjua AA, Laskey D, Delaney ML, et al. Diversity of the gut microbiota and eczema in early life. Clin Mol Allergy (2008) 6:11. doi:10.1186/1476-7961-6-11
93. Yap GC, Loo EX, Aw M, Lu Q, Shek LP, Lee BW. Molecular analysis of infant fecal microbiota in an Asian at-risk cohort-correlates with infant and childhood eczema. BMC Res Notes (2014) 7:166. doi:10.1186/1756-0500-7-166
94. Harder T, Bergmann R, Kallischnigg G, Plagemann A. Duration of breastfeeding and risk of overweight. A meta-analysis. Am J Epidemiol (2005) 162:397-403. doi:10.1093/aje/kwi222
95. Fouhy F, Guinane CM, Hussey S, Wall R, Ryan CA, Dempsey EM, et al. High-throughput sequencing reveals the incomplete, short-term recovery of infant gut microbiota following parenteral antibiotic treatment with ampicillin and gentamicin. Antimicrob Agents Chemother (2012) 56:5811-20. doi:10.1128/AAC.00789-12
96. Fouhy F, Ross RP, Fitzgerald G, Stanton C, Cotter PD. Composition of the early intestinal microbiota: knowledge, knowledge gaps and the use of high-throughput sequencing to address these gaps. Gut Microbes (2012) 3(3):203-20. doi:10.4161/gmic.20169
97. Abrahamsson TR, Rautava S, Moore AM, Neu J, Sherman PM. The time for a confirmative necrotizing enterocolitis probiotics prevention trial in extremely low birth weight infant in North America is now. J Paediatr (2014) 165:389-94. doi:10.1016/j.jpeds.2014.05.012
98. Daley D. The evolution of the hygiene hypothesis: the role of early life exposures to viruses and microbes and their relationship to asthma and allergic diseases. Curr Opin Allergy Clin Immunol (2014) 14(5):390-6. doi:10.1097/ACI.0000000000000101
99. Kalliomäki M, Antoine J-M, Herz U, Rijkers TG, Wells JM, Mercenier A. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr (2010) 140:713S-21S. doi:10.3945/jn.109.113761
100. Isolauri E, Rautava S, Salminen S. Probiotics in the development and treatment of allergic disease. Gastroenterol Clin North Am (2012) 41:747-62. doi:10.1016/j.gtc.2012.08.007
101. Toh ZQ, Anzela A, Tang ML, Licciardi PV. Probiotic therapy as a novel approach for allergic disease. Front Pharmacol (2012) 3:171. doi:10.3389/fphar.2012.00171
102. Ismail IH, Licciardi PV, Tang ML. Probiotic effect in allergic disease. J Paediatr Child Health (2013) 49:709-15. doi:10.1111/jpc.12175