Probiotics for Prevention and Treatment of Bronchial Asthma: A Systematic Review_Chinese Journal of Evidence-Based Medicine

Authors：

HE Min ¹ , WANG Ting ¹ , ZHANG Hongping ² , JIA Chune ² , XIONG Xingyu ¹ , WANG Gang ² ,  JI Yulin ¹

1. Department of Respiratory and Critical Care Medicine, West China Hospital, Sichuan University, Chengdu 610041, China; 2. Pneumology Group, Department of Integrated Traditional Chinese and Western Medicine, West China Hospital, Sichuan University, Chengdu 610041, China;

Corresponding author：

JI Yulin, Email: jiyulin@263.net

Keywords：

Probiotics; Prevention; Treatment; Bronchial asthma; Systematic review; Meta-analysis

DOI：

10.7507/1672-2531.20120072

Video：

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Objective 　To systematically assess the efficacy and safety of probiotics in prevention and treatment of bronchial asthma.
Methods 　Randomized controlled trials (RCTs) of probiotics in prevention/treatment of asthma compared with placebo were searched in PubMed, EMbase, Web of Science, OVID and The Cochrane Library published before August 2011. The quality of the included RCTs was evaluated and the data were extracted by two assessors independently. Meta-analyses were performed with RevMan 5.1 software.
Results 　Eleven RCTs on probiotics preventing asthma (n=3 656) and 5 RCTs on probiotics treating asthma (n=430) were identified. The Meta-analyses on preventing asthma showed that probiotics didn’t statistically decease the incidence of asthma (RR=0.76, 95%CI 0.47 to 1.22, P=0.25) and asthma-like wheezing (RR=0.92, 95%CI 0.62 to 1.39, P=0.71) compared with placebo. The Meta-analyses on treating asthma indicated that probiotics could prolong free episodes of asthma (RR=1.48, 95%CI 1.20 to 1.76, P lt;0.000 1) in comparison with placebo. No severe adverse events were found in all included studies.
Conclusion 　The present evidence is not b enough to prove that probiotics is effective to prevent asthma, but it may prolong free episodes of asthma. Although it seems to have the effect on improving lung function, it fails to reduce the acute onset of asthma and has no have the advantage of improving immune function.

Citation： HE Min,WANG Ting,ZHANG Hongping,JIA Chune,XIONG Xingyu,WANG Gang,JI Yulin. Probiotics for Prevention and Treatment of Bronchial Asthma: A Systematic Review. Chinese Journal of Evidence-Based Medicine, 2012, 12(4): 460-469. doi: 10.7507/1672-2531.20120072 Copy

1.	Braman SS. The global burden of asthma. Chest, 2006, 130(suppl): 4S-12S.
2.	Rhodes L, Bailey CM, Moorman JE. Asthma prevalence and control characteristics by race/ethnicity—United States, 2002. MMWR Morb Mortal Wkly Rep, 2004, 53(4): 145-148.
3.	Osborn DA, Sinn JK. Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database of Systematic Reviews 2007, Issue 4. Art. No.: CD006475. DOI: 10.1002/14651858.CD006475.pub2.
4.	Strachan DP. Hay fever, hygiene, and household size. BMJ, 1989, 299(15): 1259-1260.
5.	Sudo N, Sawamura S, Tanaka K, et al. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol, 1997, 159(25): 1739-1745.
6.	BjÖrkstén B, Sepp E, Julge K, et al. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol, 2001, 108(18): 516-520.
7.	Noverr MC, Huffnagle GB. The ‘‘microflora hypothesis’’ of allergic diseases. Clin Exp Allergy, 2005, 35(7): 1511-1520.
8.	Newburg DS. Oligosaccharides in human milk and bacterial colonization. J Pediatr Gastroenterol Nutr, 2000, 30(suppl 2): S8-17.
9.	Martinez FD, Holt PG. Role of microbial burden in aetiology of allergy and asthma. Lancet, 1999, 354(suppl 2): 12-15.
10.	Sanfilippo L, Li CK, Seth R, et al. Bacteroides fragilis enterotoxin induces the expression of IL-8 and transforming growth factor-beta (TGF-beta) by human colonic epithelial cells. Clin Exp Immunol, 2000, 119(6): 456-463.
11.	Gaskins HR. Immunological aspects of host/microbiota interactions at the intestinal epithelium. In: Mackie RI, White BA, Isaacson RE, eds.Gastrointestinal microbiology. New York: International Thomson Publishing, 1997: 537–587.
12.	Salminen S, Bouley C, Boutron-Ruault MC, et al. Functional food science and gastrointestinal physiology and function. Br J Nutr, 1998, 80 (suppl 1): 147-171.
13.	Guarner F, Schaafsma GJ. Probiotics. International Journal of Food Microbiology, 1998, 39(16): 237-238.
14.	Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol, 1997, 99(4): 179-185.
15.	Viljanen M, Savilahti E, Haahtela T, et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy, 2005, 60(5): 494-500.
16.	Rosenfeldt V, Benfeldt E, Nielsen SD, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol, 2003, 111(2): 389-395.
17.	Weston S, HalbertA, Richmond P, et al. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child, 2005, 90(7): 892-897.
18.	Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med, 2007, 175(16): 561-569.
19.	Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011].The Cochrane Collaboration, 2011. Available from www.cochranehandbook.org.
20.	van der Aa LB, van Aalderen WMC, Heymans HSA, et al. Synbiotics prevent asthma-like symptoms in infants with atopic dermatitis. Allergy, 2011, 66(10): 170-177.
21.	Kukkonen K, Savilahti E, Haahtela T, et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: A randomized, double-blind, placebo-controlled trial. Journal of Allergy and Clinical Immunology, 2007, 119(8): 192-198.
22.	Kuitunen M, Kukkonen K, Juntunen-Backman K, et al. Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. Journal of Allergy and Clinical Immunology, 2009, 123(3): 335-341.
23.	Kalliomäki M, Salminen S, Arvilommi H, et al. Probiotics in primary prevention of atopic disease: a randomized placebo-controlled trial. Lancet, 2001, 357(6): 1076-1079.
24.	Kukkonen AK, Kuitunen M, Savilahti E, et al. Airway inflammation in probiotic-treated children at 5 years. Pediatr Allergy and Immunol, 2011, 22(4): 249-251.
25.	Dotterud CK, Storrø O, Johnsen R, et al. Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. British Journal of Dermatology, 2010, 163(15): 616-623.
26.	Taylor A, Hale J, Wiltschut J, et al. Evaluation of the effects of probiotic supplementation from the neonatal period on innate immune development in infancy. Clinical and Experimental Allergy, 2006, 36(12): 1218-1226.
27.	Abrahamsson TR, Jakobsson T, Bottcher MF, et al. Probiotics in prevention of IgE-associated eczema: A double-blind, randomized,placebo-controlled trial. Journal of Allergy and Clinical Immunology, 2007, 119(15): 1174-1180.
28.	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. Journal of Allergy and Clinical Immunology, 2007, 119(15): 184-191.
29.	Kopp MV, Hennemuth I, Heinzmann A, et al. Randomized, Double-Blind, Placebo-Controlled Trial of Probiotics for Primary Prevention: No Clinical Effects of Lactobacillus GG Supplementation. Pediatrics, 2008, 121(4): 850-856.
30.	Arslanoglu S, Moro GE, Schmitt J, et al. Early Dietary Intervention with a Mixture of Prebiotic Oligosaccharides Reduces the Incidence of Allergic Manifestations and Infections during the First Two Years of Life. The Journal of Nutrition, 2008, 138(6): 1091-1095.
31.	van de Pol MA, Lutter R, Smids BS, et al. Synbiotics reduce allergen-induced T-helper 2 response and improve peak expiratory flow in allergic asthmatics. Allergy, 2011, 66(31): 39-47.
32.	Rose MA, Stieglitz F, K?ksal A, et al. Efficacy of probiotic Lactobacillus GG on allergic sensitization and asthma in infants at risk. Clinical & Experimental Allergy, 2010, 67(40): 1398-1405.
33.	Chen YS, Jan RL, Lin LY, et al. Randomized Placebo-Controlled Trial of Lactobacillus on Asthmatic Children With Allergic Rhinitis. Pediatric Pulmonology, 2010, 54(45): 1111-1120.
34.	Giovannini M, Agostoni C, Riva E, et al. A Randomized Prospective Double Blind Controlled Trial on Effects of Long-Term Consumption of Fermented Milk Containing Lactobacillus casei in Pre-School Children With Allergic Asthma and/or Rhinitis. Pediatric Research, 2007, 51(62): 215-220.
35.	Gutkowski P, Madalinski K, Grek M, et al. Effect of orally administered probiotic strains Lactobacillus and Bifidobacterium in children with atopic asthma. Centr Eur J Immunol, 2010, 35(4): 233-238.
36.	Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut? Trends Microbiol, 2004, 12(6): 562-568.
37.	Penders J, Stobberingh EE, van den Brandt PA, et al. The role of the intestinal microbiota in the development of atopic disorders. Allergy, 2007, 62(7): 1223-1236.
38.	Feleszko W, Jaworska J, Hamelmann E. Toll-like receptors: novel targets in allergic airway disease (probiotics, friends and relatives). Eur J Pharmacol, 2006, 533(12): 308-318.

1. Braman SS. The global burden of asthma. Chest, 2006, 130(suppl): 4S-12S.
2. Rhodes L, Bailey CM, Moorman JE. Asthma prevalence and control characteristics by race/ethnicity—United States, 2002. MMWR Morb Mortal Wkly Rep, 2004, 53(4): 145-148.
3. Osborn DA, Sinn JK. Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database of Systematic Reviews 2007, Issue 4. Art. No.: CD006475. DOI: 10.1002/14651858.CD006475.pub2.
4. Strachan DP. Hay fever, hygiene, and household size. BMJ, 1989, 299(15): 1259-1260.
5. Sudo N, Sawamura S, Tanaka K, et al. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol, 1997, 159(25): 1739-1745.
6. BjÖrkstén B, Sepp E, Julge K, et al. Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol, 2001, 108(18): 516-520.
7. Noverr MC, Huffnagle GB. The ‘‘microflora hypothesis’’ of allergic diseases. Clin Exp Allergy, 2005, 35(7): 1511-1520.
8. Newburg DS. Oligosaccharides in human milk and bacterial colonization. J Pediatr Gastroenterol Nutr, 2000, 30(suppl 2): S8-17.
9. Martinez FD, Holt PG. Role of microbial burden in aetiology of allergy and asthma. Lancet, 1999, 354(suppl 2): 12-15.
10. Sanfilippo L, Li CK, Seth R, et al. Bacteroides fragilis enterotoxin induces the expression of IL-8 and transforming growth factor-beta (TGF-beta) by human colonic epithelial cells. Clin Exp Immunol, 2000, 119(6): 456-463.
11. Gaskins HR. Immunological aspects of host/microbiota interactions at the intestinal epithelium. In: Mackie RI, White BA, Isaacson RE, eds.Gastrointestinal microbiology. New York: International Thomson Publishing, 1997: 537–587.
12. Salminen S, Bouley C, Boutron-Ruault MC, et al. Functional food science and gastrointestinal physiology and function. Br J Nutr, 1998, 80 (suppl 1): 147-171.
13. Guarner F, Schaafsma GJ. Probiotics. International Journal of Food Microbiology, 1998, 39(16): 237-238.
14. Majamaa H, Isolauri E. Probiotics: a novel approach in the management of food allergy. J Allergy Clin Immunol, 1997, 99(4): 179-185.
15. Viljanen M, Savilahti E, Haahtela T, et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy, 2005, 60(5): 494-500.
16. Rosenfeldt V, Benfeldt E, Nielsen SD, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol, 2003, 111(2): 389-395.
17. Weston S, HalbertA, Richmond P, et al. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child, 2005, 90(7): 892-897.
18. Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med, 2007, 175(16): 561-569.
19. Higgins JPT, Green S (editors). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011].The Cochrane Collaboration, 2011. Available from www.cochranehandbook.org.
20. van der Aa LB, van Aalderen WMC, Heymans HSA, et al. Synbiotics prevent asthma-like symptoms in infants with atopic dermatitis. Allergy, 2011, 66(10): 170-177.
21. Kukkonen K, Savilahti E, Haahtela T, et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: A randomized, double-blind, placebo-controlled trial. Journal of Allergy and Clinical Immunology, 2007, 119(8): 192-198.
22. Kuitunen M, Kukkonen K, Juntunen-Backman K, et al. Probiotics prevent IgE-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. Journal of Allergy and Clinical Immunology, 2009, 123(3): 335-341.
23. Kalliomäki M, Salminen S, Arvilommi H, et al. Probiotics in primary prevention of atopic disease: a randomized placebo-controlled trial. Lancet, 2001, 357(6): 1076-1079.
24. Kukkonen AK, Kuitunen M, Savilahti E, et al. Airway inflammation in probiotic-treated children at 5 years. Pediatr Allergy and Immunol, 2011, 22(4): 249-251.
25. Dotterud CK, Storrø O, Johnsen R, et al. Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. British Journal of Dermatology, 2010, 163(15): 616-623.
26. Taylor A, Hale J, Wiltschut J, et al. Evaluation of the effects of probiotic supplementation from the neonatal period on innate immune development in infancy. Clinical and Experimental Allergy, 2006, 36(12): 1218-1226.
27. Abrahamsson TR, Jakobsson T, Bottcher MF, et al. Probiotics in prevention of IgE-associated eczema: A double-blind, randomized,placebo-controlled trial. Journal of Allergy and Clinical Immunology, 2007, 119(15): 1174-1180.
28. 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. Journal of Allergy and Clinical Immunology, 2007, 119(15): 184-191.
29. Kopp MV, Hennemuth I, Heinzmann A, et al. Randomized, Double-Blind, Placebo-Controlled Trial of Probiotics for Primary Prevention: No Clinical Effects of Lactobacillus GG Supplementation. Pediatrics, 2008, 121(4): 850-856.
30. Arslanoglu S, Moro GE, Schmitt J, et al. Early Dietary Intervention with a Mixture of Prebiotic Oligosaccharides Reduces the Incidence of Allergic Manifestations and Infections during the First Two Years of Life. The Journal of Nutrition, 2008, 138(6): 1091-1095.
31. van de Pol MA, Lutter R, Smids BS, et al. Synbiotics reduce allergen-induced T-helper 2 response and improve peak expiratory flow in allergic asthmatics. Allergy, 2011, 66(31): 39-47.
32. Rose MA, Stieglitz F, K?ksal A, et al. Efficacy of probiotic Lactobacillus GG on allergic sensitization and asthma in infants at risk. Clinical & Experimental Allergy, 2010, 67(40): 1398-1405.
33. Chen YS, Jan RL, Lin LY, et al. Randomized Placebo-Controlled Trial of Lactobacillus on Asthmatic Children With Allergic Rhinitis. Pediatric Pulmonology, 2010, 54(45): 1111-1120.
34. Giovannini M, Agostoni C, Riva E, et al. A Randomized Prospective Double Blind Controlled Trial on Effects of Long-Term Consumption of Fermented Milk Containing Lactobacillus casei in Pre-School Children With Allergic Asthma and/or Rhinitis. Pediatric Research, 2007, 51(62): 215-220.
35. Gutkowski P, Madalinski K, Grek M, et al. Effect of orally administered probiotic strains Lactobacillus and Bifidobacterium in children with atopic asthma. Centr Eur J Immunol, 2010, 35(4): 233-238.
36. Noverr MC, Huffnagle GB. Does the microbiota regulate immune responses outside the gut? Trends Microbiol, 2004, 12(6): 562-568.
37. Penders J, Stobberingh EE, van den Brandt PA, et al. The role of the intestinal microbiota in the development of atopic disorders. Allergy, 2007, 62(7): 1223-1236.
38. Feleszko W, Jaworska J, Hamelmann E. Toll-like receptors: novel targets in allergic airway disease (probiotics, friends and relatives). Eur J Pharmacol, 2006, 533(12): 308-318.

Chinese Journal of Evidence-Based Medicine

Probiotics for Prevention and Treatment of Bronchial Asthma: A Systematic Review

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