World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics

Alessandro Fiocchi, Ruby Pawankar, Carlos Cuello-Garcia, Kangmo Ahn, Suleiman Al-Hammadi, Arnav Agarwal, Kirsten Beyer, Wesley Burks, Giorgio W Canonica, Motohiro Ebisawa, Shreyas Gandhi, Rose Kamenwa, Bee Wah Lee, Haiqi Li, Susan Prescott, John J Riva, Lanny Rosenwasser, Hugh Sampson, Michael Spigler, Luigi Terracciano, Andrea Vereda-Ortiz, Susan Waserman, Juan José Yepes-Nuñez, Jan L Brożek, Holger J Schünemann, Alessandro Fiocchi, Ruby Pawankar, Carlos Cuello-Garcia, Kangmo Ahn, Suleiman Al-Hammadi, Arnav Agarwal, Kirsten Beyer, Wesley Burks, Giorgio W Canonica, Motohiro Ebisawa, Shreyas Gandhi, Rose Kamenwa, Bee Wah Lee, Haiqi Li, Susan Prescott, John J Riva, Lanny Rosenwasser, Hugh Sampson, Michael Spigler, Luigi Terracciano, Andrea Vereda-Ortiz, Susan Waserman, Juan José Yepes-Nuñez, Jan L Brożek, Holger J Schünemann

Abstract

Background: Prevalence of allergic diseases in infants, whose parents and siblings do not have allergy, is approximately 10% and reaches 20-30% in those with an allergic first-degree relative. Intestinal microbiota may modulate immunologic and inflammatory systemic responses and, thus, influence development of sensitization and allergy. Probiotics have been reported to modulate immune responses and their supplementation has been proposed as a preventive intervention.

Objective: The World Allergy Organization (WAO) convened a guideline panel to develop evidence-based recommendations about the use of probiotics in the prevention of allergy.

Methods: We identified the most relevant clinical questions and performed a systematic review of randomized controlled trials of probiotics for the prevention of allergy. We followed the Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach to develop recommendations. We searched for and reviewed the evidence about health effects, patient values and preferences, and resource use (up to November 2014). We followed the GRADE evidence-to-decision framework to develop recommendations.

Results: Currently available evidence does not indicate that probiotic supplementation reduces the risk of developing allergy in children. However, considering all critical outcomes in this context, the WAO guideline panel determined that there is a likely net benefit from using probiotics resulting primarily from prevention of eczema. The WAO guideline panel suggests: a) using probiotics in pregnant women at high risk for having an allergic child; b) using probiotics in women who breastfeed infants at high risk of developing allergy; and c) using probiotics in infants at high risk of developing allergy. All recommendations are conditional and supported by very low quality evidence.

Conclusions: WAO recommendations about probiotic supplementation for prevention of allergy are intended to support parents, clinicians and other health care professionals in their decisions whether to use probiotics in pregnancy and during breastfeeding, and whether to give them to infants.

Keywords: Allergy; GRADE; Practice guidelines; Prevention; Probiotics.

References

    1. Haahtela T, von Hertzen L, Makela M, Hannuksela M. Allergy Programme Working G: Finnish Allergy Programme 2008–2018–time to act and change the course. Allergy. 2008;63:634–45. doi: 10.1111/j.1398-9995.2008.01712.x.
    1. Prescott SL, Dunstan JA, Hale J, Breckler L, Lehmann H, Weston S, Richmond P. Clinical effects of probiotics are associated with increased interferon-gamma responses in very young children with atopic dermatitis. Clin Exp Allergy. 2005;35:1557–64. doi: 10.1111/j.1365-2222.2005.02376.x.
    1. Arshad SH, Kurukulaaratchy RJ, Fenn M, Matthews S. Early life risk factors for current wheeze, asthma, and bronchial hyperresponsiveness at 10 years of age. Chest. 2005;127:502–8. doi: 10.1378/chest.127.2.502.
    1. Agostoni C, Axelsson I, Goulet O, Koletzko B, Michaelsen KF, Puntis JW, Rigo J, Shamir R, Szajewska H, Turck D. Prebiotic oligosaccharides in dietetic products for infants: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr. 2004;39:465–73. doi: 10.1097/00005176-200411000-00003.
    1. Shreiner A, Huffnagle GB, Noverr MC. The "Microflora Hypothesis" of allergic disease. Adv Exp Med Biol. 2008;635:113–34. doi: 10.1007/978-0-387-09550-9_10.
    1. Isolauri E, Sutas Y, Kankaanpaa P, Arvilommi H, Salminen S. Probiotics: effects on immunity. Am J Clin Nutr. 2001;73:444S–50S.
    1. Fiocchi A, Burks W, Bahna SL, Bielory L, Boyle RJ, Cocco R, Dreborg S, Goodman R, Kuitunen M, Haahtela T, et al. Clinical use of probiotics in pediatric allergy (CUPPA): A world allergy organization position paper. World Allergy Organ J. 2012;5:148–67. doi: 10.1097/WOX.0b013e3182784ee0.
    1. Technological & Commercial Applications of Lactic Acid Bacteria; Health & Nutritional Benefits in Dairy Products []
    1. Boyce JA, Assa'ad A, Burks AW, Jones SM, Sampson HA, Wood RA, Plaut M, Cooper SF, Fenton MJ, Arshad SH, 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. 2010;126:S1–58. doi: 10.1016/j.jaci.2010.10.008.
    1. Agostoni C, Decsi T, Fewtrell M, Goulet O, Kolacek S, Koletzko B, Michaelsen KF, Moreno L, Puntis J, Rigo J, et al. Complementary feeding: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr. 2008;46:99–110. doi: 10.1097/.
    1. Schunemann HJ, Wiercioch W, Etxeandia I, Falavigna M, Santesso N, Mustafa R, Ventresca M, Brignardello-Petersen R, Laisaar KT, Kowalski S, et al. Guidelines 2.0: systematic development of a comprehensive checklist for a successful guideline enterprise. CMAJ. 2013;186:E123–142. doi: 10.1503/cmaj.131237.
    1. GRADEpro Guideline Development Tool (G2DT): Brożek J, Nowak A, Kunstman P, Schünemann HJ. (Computer Program) Version 2.xx. (Available from: ). In Book GRADEpro Guideline Development Tool (G2DT): Brożek J, Nowak A, Kunstman P, Schünemann HJ. (Computer Program) Version 2.xx. (Available from: ). (Editor ed.^eds.). City; 2014.
    1. Guyatt GH, Oxman AD, Kunz R, Atkins D, Brozek J, Vist G, Alderson P, Glasziou P, Falck-Ytter Y, Schunemann HJ. GRADE guidelines: 2. Framing the question and deciding on important outcomes. J Clin Epidemiol. 2011;64:395–400. doi: 10.1016/j.jclinepi.2010.09.012.
    1. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 []
    1. Azad MB, Coneys JG, Kozyrskyj AL, Field CJ, Ramsey CD, Becker AB, Friesen C, Abou-Setta AM, Zarychanski R. Probiotic supplementation during pregnancy or infancy for the prevention of asthma and wheeze: systematic review and meta-analysis. BMJ. 2013;347:f6471. doi: 10.1136/bmj.f6471.
    1. Betsi GI, Papadavid E, Falagas ME. Probiotics for the treatment or prevention of atopic dermatitis: a review of the evidence from randomized controlled trials. Am J Clin Dermatol. 2008;9:93–103. doi: 10.2165/00128071-200809020-00002.
    1. Doege K, Grajecki D, Zyriax BC, Detinkina E, Zu Eulenburg C, Buhling KJ. Impact of maternal supplementation with probiotics during pregnancy on atopic eczema in childhood–a meta-analysis. Br J Nutr. 2012;107:1–6. doi: 10.1017/S0007114511003400.
    1. Dugoua JJ, Machado M, Zhu X, Chen X, Koren G, Einarson TR. Probiotic safety in pregnancy: a systematic review and meta-analysis of randomized controlled trials of Lactobacillus, Bifidobacterium, and Saccharomyces spp. J Obstet Gynaecol Can. 2009;31:542–52.
    1. Elazab N, Mendy A, Gasana J, Vieira ER, Quizon A, Forno E. Probiotic administration in early life, atopy, and asthma: a meta-analysis of clinical trials. Pediatrics. 2013;132:e666–676. doi: 10.1542/peds.2013-0246.
    1. Foolad N, Brezinski EA, Chase EP, Armstrong AW. Effect of nutrient supplementation on atopic dermatitis in children: a systematic review of probiotics, prebiotics, formula, and fatty acids. JAMA Dermatol. 2013;149:350–5. doi: 10.1001/jamadermatol.2013.1495.
    1. 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;121:116–121. doi: 10.1016/j.jaci.2007.10.043.
    1. Pelucchi C, Chatenoud L, Turati F, Galeone C, Moja L, Bach JF, La Vecchia C. Probiotics supplementation during pregnancy or infancy for the prevention of atopic dermatitis: a meta-analysis. Epidemiology. 2012;23:402–14. doi: 10.1097/EDE.0b013e31824d5da2.
    1. Boyle RJ, Ismail IH, Kivivuori S, Licciardi PV, Robins-Browne RM, Mah LJ, Axelrad C, Moore S, Donath S, Carlin JB, et al. Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial. Allergy. 2011;66:509–16. doi: 10.1111/j.1398-9995.2010.02507.x.
    1. Dotterud CK, Storro O, Johnsen R, Oien T. Probiotics in pregnant women to prevent allergic disease: a randomized, double-blind trial. Br J Dermatol. 2010;163:616–23. doi: 10.1111/j.1365-2133.2010.09889.x.
    1. Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: A double-blind placebo-controlled study. Clin Exp Allergy. 2008;38:1342–8. doi: 10.1111/j.1365-2222.2008.03008.x.
    1. Kim JY, Kwon JH, Ahn SH, Lee SI, Han YS, Choi YO, Lee SY, Ahn KM, Ji GE. 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:e386–93. doi: 10.1111/j.1399-3038.2009.00958.x.
    1. Rautava S, Kalliomaki M, Isolauri E. Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol. 2002;109:119–21. doi: 10.1067/mai.2002.120273.
    1. 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. 2012;130:1355–60. doi: 10.1016/j.jaci.2012.09.003.
    1. Abrahamsson TR, Jakobsson T, Bottcher MF, Fredrikson M, Jenmalm MC, Bjorksten B, Oldaeus G. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol. 2007;119:1174–80. doi: 10.1016/j.jaci.2007.01.007.
    1. Allen SJ, Jordan S, Storey M, Thornton CA, Gravenor MB, Garaiova I, Jones RH, Macfarlane TV, Seager AL, Manshian B, et al. Probiotics and atopic ECZEMA: A double-blind randomised controlled trial. Arch Dis Child. 2012;97:A2. doi: 10.1136/archdischild-2012-301885.5.
    1. Allen SJ, Jordan S, Storey M, Thornton CA, Gravenor M, Garaiova I, Plummer SF, Wang D, Morgan G. Dietary supplementation with lactobacilli and bifidobacteria is well tolerated and not associated with adverse events during late pregnancy and early infancy. J Nutr. 2010;140:483–8. doi: 10.3945/jn.109.117093.
    1. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. Lancet. 2001;357:1076–9. doi: 10.1016/S0140-6736(00)04259-8.
    1. 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. doi: 10.1016/S0140-6736(03)13490-3.
    1. 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:e850–856. doi: 10.1542/peds.2007-1492.
    1. Kuitunen M, Kukkonen K, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Haahtela T, Savilahti E. 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. doi: 10.1016/j.jaci.2008.11.019.
    1. Kukkonen AK, Kuitunen M, Savilahti E, Pelkonen A, Malmberg P, Makela M. Airway inflammation in probiotic-treated children at 5 years. Pediatr Allergy Immunol. 2011;22:249–51. doi: 10.1111/j.1399-3038.2010.01079.x.
    1. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M. 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. doi: 10.1016/j.jaci.2006.09.009.
    1. Marschan E, Kuitunen M, Kukkonen K, Poussa T, Sarnesto A, Haahtela T, Korpela R, Savilahti E, Vaarala O. Probiotics in infancy induce protective immune profiles that are characteristic for chronic low-grade inflammation. Clin Exp Allergy. 2008;38:611–8. doi: 10.1111/j.1365-2222.2008.02942.x.
    1. Niers L, Martin R, Rijkers G, Sengers F, Timmerman H, van Uden N, Smidt H, Kimpen J, Hoekstra M. The effects of selected probiotic strains on the development of eczema (the PandA study) Allergy. 2009;64:1349–58. doi: 10.1111/j.1398-9995.2009.02021.x.
    1. Ou CY, Kuo HC, Wang L, Hsu TY, Chuang H, Liu CA. Prenatal and postnatal probiotics reduces maternal but not childhood allergic diseases: A randomized, double-blind, placebo-controlled trial. Clin Exp Allergy. 2012;42:1386–96. doi: 10.1111/j.1365-2222.2012.04037.x.
    1. Wickens K, Black PN, Stanley TV, Mitchell E, Fitzharris P, Tannock GW, Purdie G, Crane J, 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. 2008;122:788–94. doi: 10.1016/j.jaci.2008.07.011.
    1. Wickens K, Black P, Stanley TV, Mitchell E, Barthow C, Fitzharris P, et al. A protective effect of Lactobacillus rhamnosus HN001 against eczema in the first 2 years of life persists to age 4 years. Clin Exp Allergy. 2012;42(7):1071-9.
    1. Kalliomaki 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. 2007;119:1019–21. doi: 10.1016/j.jaci.2006.12.608.
    1. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JNV, Shanman R, Johnsen B, Shekelle PG. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: A systematic review and meta-analysis. JAMA. 2012;307:1959–69. doi: 10.1001/jama.2012.3507.
    1. Muraro A, Halken S, Arshad SH, Beyer K, Dubois AE, Du Toit G, Eigenmann PA, Grimshaw KE, Hoest A, Lack G, et al. EAACI food allergy and anaphylaxis guidelines. Primary prevention of food allergy. Allergy. 2014;69:590–601. doi: 10.1111/all.12398.
    1. Braegger C, Chmielewska A, Decsi T, Kolacek S, Mihatsch W, Moreno L, Piescik M, Puntis J, Shamir R, Szajewska H, 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. 2011;52:238–50. doi: 10.1097/MPG.0b013e3181fb9e80.
    1. Guarner F, Khan AG, Garisch J, Eliakim R, Gangl A, Thomson A, Krabshuis J, Lemair T, Kaufmann P, de Paula JA, et al. World Gastroenterology Organisation Global Guidelines: probiotics and prebiotics October 2011. J Clin Gastroenterol. 2012;46:468–81. doi: 10.1097/MCG.0b013e3182549092.
    1. Morelli L, Capurso L. FAO/WHO guidelines on probiotics: 10 years later. J Clin Gastroenterol. 2012;46(Suppl):S1–2. doi: 10.1097/MCG.0b013e318269fdd5.
    1. Ortiz-Andrellucchi A, Sanchez-Villegas A, Rodriguez-Gallego C, Lemes A, Molero T, Soria A, Pena-Quintana L, Santana M, Ramirez O, Garcia J, et al. Immunomodulatory effects of the intake of fermented milk with Lactobacillus casei DN114001 in lactating mothers and their children. Br J Nutr. 2008;100:834–45. doi: 10.1017/S0007114508959183.
    1. Foisy M, Boyle RJ, Chalmers JR, Simpson EL, Williams HC. Overview of Reviews The prevention of eczema in infants and children: an overview of Cochrane and non-Cochrane reviews. Evid Based Child Health. 2011;6:1322–39. doi: 10.1002/ebch.827.
    1. Mugambi MN, Musekiwa A, Lombard M, Young T, Blaauw R. Synbiotics, probiotics or prebiotics in infant formula for full term infants: a systematic review. Nutr J. 2012;11:81. doi: 10.1186/1475-2891-11-81.
    1. Osborn DA, Sinn JK: Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database Syst Rev 2007:CD006475.
    1. Hascoet JM, Hubert C, Rochat F, Legagneur H, Gaga S, Emady-Azar S, Steenhout PG. Effect of formula composition on the development of infant gut microbiota. J Pediatr Gastroenterol Nutr. 2011;52:756–62. doi: 10.1097/MPG.0b013e3182105850.
    1. Lodinova-Zadnikova R, Prokesova L, Kocourkova I, Hrdy J, Zizka J. Prevention of allergy in infants of allergic mothers by probiotic Escherichia coli. Int Arch Allergy Immunol. 2010;153:201–6. doi: 10.1159/000312638.
    1. Morisset M, Aubert-Jacquin C, Soulaines P, Moneret-Vautrin DA, Dupont C. A non-hydrolyzed, fermented milk formula reduces digestive and respiratory events in infants at high risk of allergy. Eur J Clin Nutr. 2011;65:175–83. doi: 10.1038/ejcn.2010.250.
    1. Prescott SL, Wiltschut J, Taylor A, Westcott L, Jung W, Currie H, Dunstan JA. Early markers of allergic disease in a primary prevention study using probiotics: 2.5-year follow-up phase. Allergy. 2008;63:1481–90. doi: 10.1111/j.1398-9995.2008.01778.x.
    1. Soh SE, Aw M, Gerez I, Chong YS, Rauff M, Ng YP, Wong HB, Pai N, Lee BW, Shek LP. 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. 2009;39:571–8. doi: 10.1111/j.1365-2222.2008.03133.x.
    1. Taylor AL, Hale J, Hales BJ, Dunstan JA, Thomas WR, Prescott SL. 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. 2007;18:10–9. doi: 10.1111/j.1399-3038.2006.00483.x.
    1. West CE, Hammarstrom ML, Hernell O. Probiotics during weaning reduce the incidence of eczema. Pediatr Allergy Immunol. 2009;20:430–7. doi: 10.1111/j.1399-3038.2009.00745.x.
    1. Bertazzoni E, Donelli G, Midtvedt T, Nicoli J, Sanz Y. Probiotics and clinical effects: is the number what counts? J Chemother. 2013;25:193–212. doi: 10.1179/1973947813Y.0000000078.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera