DOI QR코드

DOI QR Code

Clinical efficacy and mechanism of probiotics in allergic diseases

  • Kim, Ha-Jung (Asan Institute for Life Sciences, University of Ulsan College of Medicine) ;
  • Kim, Hyung Young (Department of Pediatrics, Kosin University College of Medicine) ;
  • Lee, So-Yeon (Department of Pediatrics, Hallym University Sacred Heart Hospital, Hallym University College of Medicine) ;
  • Seo, Ju-Hee (Department of Pediatrics, Korea Cancer Center Hospital) ;
  • Lee, Eun (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Hong, Soo-Jong (Department of Pediatrics, Childhood Asthma Atopy Center, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2013.05.03
  • Accepted : 2013.06.11
  • Published : 2013.09.15

Abstract

A complex interplay between genetic and environmental factors partially contributes to the development of allergic diseases by affecting development during prenatal and early life. To explain the dramatic increase in the prevalence of allergic diseases, the hygiene hypothesis proposed that early exposure to infection prevented allergic diseases. The hygiene hypothesis has changed to the microbial hypothesis, in which exposure to microbes is closely linked to the development of the early immune system and allergic diseases. The intestinal flora may contribute to allergic disease through its substantial effect on mucosal immunity. Based on findings that exposure to microbial flora early in life can change the Th1/Th2 balance, thus favoring a Th1 cell response, probiotics may be beneficial in preventing allergic diseases. However, evidence from clinical and basic research to prove the efficacy of probiotics in preventing allergy is lacking. To date, studies have yielded inconsistent findings on the usefulness of probiotics in allergic diseases. It is difficult to demonstrate an exact effect of probiotics on asthma, allergic rhinitis, and food allergy because of study limitations, such as different first supplementation period, duration, different strains, short follow-up period, and host factors. However, many studies have demonstrated a significant clinical improvement in atopic dermatitis with the use of probiotics. An accurate understanding of the development of human immunity, intestinal barrier function, intestinal microbiota, and systemic immunity is required to comprehend the effects of probiotics on allergic diseases.

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr 2007;27:363-88. https://doi.org/10.1146/annurev.nutr.27.061406.093705
  2. Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med 2009;27:358-68. https://doi.org/10.1055/s-0029-1237424
  3. Strachan DP. Family size, infection and atopy: the first decade of the "hygiene hypothesis". Thorax 2000;55 Suppl 1:S2-10. https://doi.org/10.1136/thorax.55.suppl_1.S2
  4. Lee SY, Kwon JW, Seo JH, Song YH, Kim BJ, Yu J, et al. Prevalence of atopy and allergic diseases in Korean children: associations with a farming environment and rural lifestyle. Int Arch Allergy Immunol 2012;158:168-74. https://doi.org/10.1159/000330820
  5. Strachan DP. Hay fever, hygiene, and household size. BMJ 1989; 299:1259-60. https://doi.org/10.1136/bmj.299.6710.1259
  6. Lee E, Lee SY, Ahn KM, Kim KW, Shin YH, Hong SJ. Interactions between CD14/IL-13 genes and caesarean section delivery may affect the development of atopic dermatitis in a COCOA study. Poster presented at: 2013 Annual Meeting of AAAAI; 2013 Feb 22- 26; San Diego, USA. Milwaukee: American Academy of Allergy Asthma & Immunology; 2013.
  7. Eisenbarth SC, Piggott DA, Huleatt JW, Visintin I, Herrick CA, Bottomly K. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J Exp Med 2002;196:1645-51. https://doi.org/10.1084/jem.20021340
  8. Perzanowski MS, Miller RL, Thorne PS, Barr RG, Divjan A, Sheares BJ, et al. Endotoxin in inner-city homes: associations with wheeze and eczema in early childhood. J Allergy Clin Immunol 2006;117:1082-9. https://doi.org/10.1016/j.jaci.2005.12.1348
  9. Blaser MJ, Falkow S. What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 2009;7:887-94. https://doi.org/10.1038/nrmicro2245
  10. Iacono A, Raso GM, Canani RB, Calignano A, Meli R. Probiotics as an emerging therapeutic strategy to treat NAFLD: focus on molecular and biochemical mechanisms. J Nutr Biochem 2011;22: 699-711. https://doi.org/10.1016/j.jnutbio.2010.10.002
  11. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002;347:911-20. https://doi.org/10.1056/NEJMra020100
  12. 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.
  13. Hyman RW, Fukushima M, Diamond L, Kumm J, Giudice LC, Davis RW. Microbes on the human vaginal epithelium. Proc Natl Acad Sci U S A 2005;102:7952-7. https://doi.org/10.1073/pnas.0503236102
  14. 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. https://doi.org/10.1073/pnas.1002601107
  15. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012;336:489-93. https://doi.org/10.1126/science.1219328
  16. Jang SO, Kim HJ, Kim YJ, Kang MJ, Kwon JW, Seo JH, et al. Asthma prevention by Lactobacillus rhamnosus in a mouse model is associated with CD4(+)CD25(+)Foxp3(+) T cells. Allergy Asthma Immunol Res 2012;4:150-6. https://doi.org/10.4168/aair.2012.4.3.150
  17. Pelucchi C, Chatenoud L, Turati F, Galeone C, Moja L, Bach JF, et al. Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis. Epidemiology 2012;23:402-14. https://doi.org/10.1097/EDE.0b013e31824d5da2
  18. Wold AE. The hygiene hypothesis revised: is the rising frequency of allergy due to changes in the intestinal flora? Allergy 1998; 53(46 Suppl):20-5.
  19. Chen CC, Chiu CH, Lin TY, Shi HN, Walker WA. Effect of probiotics Lactobacillus acidophilus on Citrobacter rodentium colitis: the role of dendritic cells. Pediatr Res 2009;65:169-75. https://doi.org/10.1203/PDR.0b013e31818d5a06
  20. 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 2009;123:335-41. https://doi.org/10.1016/j.jaci.2008.11.019
  21. Taylor AL, Dunstan JA, Prescott SL. 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 2007;119:184-91. https://doi.org/10.1016/j.jaci.2006.08.036
  22. Abrahamsson TR, Jakobsson T, Bottcher MF, Fredrikson M, Jenmalm MC, Bjorksten B, et al. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 2007;119:1174-80. https://doi.org/10.1016/j.jaci.2007.01.007
  23. Kopp MV, 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 2008;121:e850-6. https://doi.org/10.1542/peds.2007-1492
  24. Kalliomaki 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 2003;361:1869-71. https://doi.org/10.1016/S0140-6736(03)13490-3
  25. van der Aa LB, van Aalderen WM, Heymans HS, Henk Sillevis Smitt J, Nauta AJ, Knippels LM, et al. Synbiotics prevent asthma-like symptoms in infants with atopic dermatitis. Allergy 2011;66:170-7. https://doi.org/10.1111/j.1398-9995.2010.02416.x
  26. Chen YS, Jan RL, Lin YL, Chen HH, Wang JY. Randomized placebo-controlled trial of lactobacillus on asthmatic children with allergic rhinitis. Pediatr Pulmonol 2010;45:1111-20. https://doi.org/10.1002/ppul.21296
  27. Lenoir-Wijnkoop I, Sanders ME, Cabana MD, Caglar E, Corthier G, Rayes N, et al. Probiotic and prebiotic influence beyond the intestinal tract. Nutr Rev 2007;65:469-89. https://doi.org/10.1111/j.1753-4887.2007.tb00272.x
  28. Ouwehand AC, Nermes M, Collado MC, Rautonen N, Salminen S, Isolauri E. Specific probiotics alleviate allergic rhinitis during the birch pollen season. World J Gastroenterol 2009;15:3261-8. https://doi.org/10.3748/wjg.15.3261
  29. Wassenberg J, Nutten S, Audran R, Barbier N, Aubert V, Moulin J, et al. Effect of Lactobacillus paracasei ST11 on a nasal provocation test with grass pollen in allergic rhinitis. Clin Exp Allergy 2011;41:565-73. https://doi.org/10.1111/j.1365-2222.2011.03695.x
  30. Rose MA, Stieglitz F, Koksal A, Schubert R, Schulze J, Zielen S. Efficacy of probiotic Lactobacillus GG on allergic sensitization and asthma in infants at risk. Clin Exp Allergy 2010;40:1398-405. https://doi.org/10.1111/j.1365-2222.2010.03560.x
  31. Ivory K, Chambers SJ, Pin C, Prieto E, Arques JL, Nicoletti C. Oral delivery of Lactobacillus casei Shirota modifies allergeninduced immune responses in allergic rhinitis. Clin Exp Allergy 2008;38:1282-9. https://doi.org/10.1111/j.1365-2222.2008.03025.x
  32. Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy 2002;57:243-6. https://doi.org/10.1034/j.1398-9995.2002.1s3299.x
  33. Koyama T, Kirjavainen PV, Fisher C, Anukam K, Summers K, Hekmat S, et al. Development and pilot evaluation of a novel probiotic mixture for the management of seasonal allergic rhinitis. Can J Microbiol 2010;56:730-8. https://doi.org/10.1139/W10-061
  34. Fiocchi A, Burks W, Bahna SL, Bielory L, Boyle RJ, Cocco R, et al. Clinical use of probiotics in pediatric allergy (CUPPA): a world allergy organization position paper. World Allergy Organ J 2012;5:148-167. https://doi.org/10.1097/WOX.0b013e3182784ee0
  35. Kim H, Kwack K, Kim DY, Ji GE. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin-induced allergy mouse model. FEMS Immunol Med Microbiol 2005;45:259-67. https://doi.org/10.1016/j.femsim.2005.05.005
  36. Osborn DA, Sinn JK. Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database Syst Rev 2007;(4):CD006475.
  37. Drago L, Iemoli E, Rodighiero V, Nicola L, De Vecchi E, Piconi S. Effects of Lactobacillus salivarius LS01 (DSM 22775) treatment on adult atopic dermatitis: a randomized placebo-controlled study. Int J Immunopathol Pharmacol 2011;24:1037-48. https://doi.org/10.1177/039463201102400421
  38. Lee J, Seto D, Bielory L. Meta-analysis of clinical trials of probiotics for prevention and treatment of pediatric atopic dermatitis. J Allergy Clin Immunol 2008;121:116-21.e11. https://doi.org/10.1016/j.jaci.2007.10.043
  39. 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 2007;119:192-8. https://doi.org/10.1016/j.jaci.2006.09.009
  40. Jenmalm MC, Duchen K. Timing of allergy-preventive and immunomodulatory dietary interventions - are prenatal, perinatal or postnatal strategies optimal? Clin Exp Allergy 2013;43:273-8. https://doi.org/10.1111/cea.12003
  41. Kim JY, Kwon JH, Ahn SH, Lee SI, Han YS, Choi YO, 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 2010;21(2 Pt 2):e386-93. https://doi.org/10.1111/j.1399-3038.2009.00958.x
  42. Kim NY, Ji GE. Effects of probiotics on the prevention of atopic dermatitis. Korean J Pediatr 2012;55:193-201. https://doi.org/10.3345/kjp.2012.55.6.193
  43. Kim HJ, Kim YJ, Kang MJ, Seo JH, Kim HY, Jeong SK, et al. A novel mouse model of atopic dermatitis with epicutaneous allergen sensitization and the effect of Lactobacillus rhamnosus. Exp Dermatol 2012;21:672-5. https://doi.org/10.1111/j.1600-0625.2012.01539.x
  44. Won TJ, Kim B, Lim YT, Song DS, Park SY, Park ES, et al. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC / Nga mice. J Appl Microbiol 2011;110:1195-202. https://doi.org/10.1111/j.1365-2672.2011.04981.x
  45. Nowak-Wegrzyn A, Muraro A. Food allergy therapy: is a cure within reach? Pediatr Clin North Am 2011;58:511-30, xii. https://doi.org/10.1016/j.pcl.2011.02.010
  46. Zhang LL, Chen X, Zheng PY, Luo Y, Lu GF, Liu ZQ, et al. Oral Bifidobacterium modulates intestinal immune inflammation in mice with food allergy. J Gastroenterol Hepatol 2010;25:928-34. https://doi.org/10.1111/j.1440-1746.2009.06193.x
  47. Schiavi E, Barletta B, Butteroni C, Corinti S, Boirivant M, Di Felice G. Oral therapeutic administration of a probiotic mixture suppresses established Th2 responses and systemic anaphylaxis in a murine model of food allergy. Allergy 2011;66:499-508. https://doi.org/10.1111/j.1398-9995.2010.02501.x
  48. Brouwer ML, Wolt-Plompen SA, Dubois AE, van der Heide S, Jansen DF, Hoijer MA, et al. No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin Exp Allergy 2006;36:899-906. https://doi.org/10.1111/j.1365-2222.2006.02513.x
  49. Hol J, van Leer EH, Elink Schuurman BE, de Ruiter LF, Samsom JN, Hop W, et al. The acquisition of tolerance toward cow's milk through probiotic supplementation: a randomized, controlled trial. J Allergy Clin Immunol 2008;121:1448-54. https://doi.org/10.1016/j.jaci.2008.03.018
  50. Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol 1997;99:179-85. https://doi.org/10.1016/S0091-6749(97)70093-9
  51. Isolauri E, Arvola T, Sutas Y, Moilanen E, Salminen S. Probiotics in the management of atopic eczema. Clin Exp Allergy 2000;30:1604-10.
  52. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 2007;37:498-505. https://doi.org/10.1111/j.1365-2222.2006.02629.x
  53. Jan RL, Yeh KC, Hsieh MH, Lin YL, Kao HF, Li PH, et al. Lactobacillus gasseri suppresses Th17 pro-inflammatory response and attenuates allergen-induced airway inflammation in a mouse model of allergic asthma. Br J Nutr 2012;108:130-9. https://doi.org/10.1017/S0007114511005265
  54. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, Sahoo A, et al. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 2010;107:2159-64. https://doi.org/10.1073/pnas.0904055107
  55. Weiss G, Christensen HR, Zeuthen LH, Vogensen FK, Jakobsen M, Frokiær H. Lactobacilli and bifidobacteria induce differential interferon-$\beta$ profiles in dendritic cells. Cytokine 2011;56:520-30. https://doi.org/10.1016/j.cyto.2011.07.024
  56. Kim HJ, Kim YJ, Lee SH, Kang MJ, Yu HS, Jung YH, et al. Effects of Lactobacillus rhamnosus on asthma with an adoptive transfer of dendritic cells in mice. J Appl Microbiol 2013 Jun 3 [Epub]. http://dx.doi.org/10.1111/jam.12268.
  57. Lee SY, Lee JY, Jang SO, Kang MJ, Song YH, Kim BJ, et al. The immunologic effects of Lactobacillus rhamnosus (Lcr35) supplements in adult patients with atopic dermatitis. Korean J Asthma Allergy Clin Immunol 2008;28:128-33.
  58. Kong DY, Yang HJ, Pyun BY. The effects on treatment of atopic dermatitis with oral Lactobacillus casei supplements in Korean children. Pediatr Allergy Respir Dis 2007;17:27-37.
  59. Yu J, Jang SO, Kim BJ, Song YH, Kwon JW, Kang MJ, et al. The effects of Lactobacillus rhamnosus on the prevention of asthma in a murine model. Allergy Asthma Immunol Res 2010;2:199-205. https://doi.org/10.4168/aair.2010.2.3.199
  60. Hong HJ, Kim E, Cho D, Kim TS. Differential suppression of heatkilled lactobacilli isolated from kimchi, a Korean traditional food, on airway hyper-responsiveness in mice. J Clin Immunol 2010;30:449-58. https://doi.org/10.1007/s10875-010-9375-8
  61. Kim JY, Choi YO, Ji GE. Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J Microbiol Biotechnol 2008;18:1393-400.
  62. Choi IS, Lim YJ, Na HS, Lee HC, Choung JT, Kook H. The effect of Lactobacillus acidophilus on the Primary prevention of asthma in a murine asthmatic model. Pediatr Allergy Respir Dis 2008;18:208-18.
  63. Park CW, Youn M, Jung YM, Kim H, Jeong Y, Lee HK, et al. New functional probiotic Lactobacillus sakei probio 65 alleviates atopic symptoms in the mouse. J Med Food 2008;11:405-12. https://doi.org/10.1089/jmf.2007.0144