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

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

doi:10.1186/s40413-015-0055-2

Cited by 473Probiotics and Fermented FoodsFood Allergy and Anaphylaxis ResearchAsthma and respiratory diseases

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

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Fiocchi, Alessandro, Pawankar, Ruby, Cuello-Garcia, Carlos, Ahn, Kangmo, Al-Hammadi, Suleiman, Agarwal, Arnav, Beyer, Kirsten, Burks, Wesley, Canonica, Giorgio W, Ebisawa, Motohiro, Gandhi, Shreyas, Kamenwa, Rose, Lee, Bee Wah, Li, Haiqi, Prescott, Susan, Riva, John J, Rosenwasser, Lanny, Sampson, Hugh, Spigler, Michael, Terracciano, Luigi, Vereda-Ortiz, Andrea, Waserman, Susan, Yepes-Nuñez, Juan José, Brożek, Jan L, Schünemann, Holger J·2015·World Allergy Organization Journal

DOI 10.1186/s40413-015-0055-2PMC PMC4307749

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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.

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WAO guidelines concluded there is currently no evidence that probiotic supplementation reduces allergy incidence in children, but there is likely a net benefit for eczema prevention.
“These guidelines concluded that currently there is no evidence supporting probiotic supplementation for reducing the risk of allergy incidence in children. However, there is likely to be a net benefit using probiotics for eczema prevention, which requires further clinical trials to increase the sample size and the reliability of the results.”
From Bifidobacteria and Their Health-Promoting Effects (2017) · cites this paper as [166]

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Emerging Priorities for Microbiome Research
Cullen, C. M., Aneja, K. K., Beyhan, S., Cho, C. E., Woloszynek, S., Convertino, M., McCoy, S. J., Zhang, Y., Anderson, M. Z., Alvarez‐Ponce, D., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00136 · Cited by 202
“Fiocchi et al. (2015) similarly reported little conﬁdence in the estimated eﬀects to recommend probiotic use for allergy prevention in children from 21 RCTs due to poor quality.”
Self-citation
The developing gut microbiota and its consequences for health
Butel, M.-J., Waligora-Dupriet, A.-J., & Wydau-Dematteis, S. (2018) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174418000119 · Cited by 182
“This led to the World Allergy Organization (WAO) to write down specific recommendations concerning this supplementation limiting it to the population at a higher risk of developing allergy.(98) Concerning prebiotic, the WAO suggests to use prebiotic supplementation in infants who are not exclusively breastfed and not…”
Background
Gut microbiota profile in children affected by atopic dermatitis and evaluation of intestinal persistence of a probiotic mixture
Reddel, S., CHIERICO, F. D., Quagliariello, A., Giancristoforo, S., Vernocchi, P., Russo, A., Fiocchi, A. G., Rossi, P., Putignani, L., & Hachem, M. E. (2019) · Scientific Reports · doi:10.1038/s41598-019-41149-6 · Cited by 184
Self-citation
Association between the gut microbiota and mineral metabolism
Skrypnik, K., & Suliburska, J. (2017) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.8724 · Cited by 182
The infant gut microbiome as a microbial organ influencing host well-being
Turroni, F., Milani, C., Duranti, S., Lugli, G. A., Bernasconi, S., Margollés, A., Pierro, F. D., van Sinderen, D., & Ventura, M. (2020) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/s13052-020-0781-0 · Cited by 176
“These guidelines concluded that, although current evidence likely supports a net benefit related to the use of probiotics in eczema prevention, there is not enough evidence supporting the recommendation of probiotics for the reduction of allergy risk in children [70].”
Background
The gut microbiome in food allergy
Zhao, W., Ho, H.-E., & Bunyavanich, S. (2019) · Annals of Allergy, Asthma & Immunology · doi:10.1016/j.anai.2018.12.012 · Cited by 160
The Microbiome, Timing, and Barrier Function in the Context of Allergic Disease
Wesemann, D. R., & Nagler‐Anderson, C. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.002 · Cited by 165
“…efficacy has largely been confined to early infancy; a meta-analysis of clinical trials determined that prenatal, or early post-natal, administration of probiotics reduced total IgE levels and the risk of atopic sensitization, but not asthma or wheezing (Elazab et al., 2013; Fiocchi et al., 2015).”
The influence of probiotics on vaccine responses—A systematic review
Zimmermann, P., & Curtis, N. (2018) · Vaccine · doi:10.1016/j.vaccine.2017.08.069 · Cited by 142
Gut Microbiota as a Target for Preventive and Therapeutic Intervention against Food Allergy
Aitoro, R., Paparo, L., Amoroso, A., Costanzo, M. D., Cosenza, L., Granata, V., Scala, C. D., Nocerino, R., Trinchese, G., Montella, M. O., et al. (2017) · Nutrients · doi:10.3390/nu9070672 · Cited by 138
“Recently published guidelines for atopic disease pr ventio fr m the World Allergy O anization concluded that there is a lik ly benefit to using probiotics in preventi g eczema in children wit a family history of allergic disease, but the vidence is v ry low in quality [85].”
Background
Vitamin D supplementation in primary allergy prevention: Systematic review of randomized and non‐randomized studies
Yepes-Núñez, J. J., Brożek, J., Fiocchi, A. G., Pawankar, R., Cuello‐García, C. A., Zhang, Y., Morgano, G. P., Agarwal, A., Gandhi, S., Terracciano, L., et al. (2017) · Allergy · doi:10.1111/all.13241 · Cited by 140
Self-citation
Human Milk and Allergic Diseases: An Unsolved Puzzle
Munblit, D., Peroni, D. G., Boix-Amorós, A., Hsu, P. S., Land, B. V., Gay, M. C. L., Kolotilina, A., Skevaki, C. L., Boyle, R. J., Collado, M. C., et al. (2017) · Nutrients · doi:10.3390/nu9080894 · Cited by 165
Clinical practice guidelines for the management of atopic dermatitis 2018
Katoh, N., Ohya, Y., Ikeda, M., Ebihara, T., Katayama, I., Saeki, H., Shimojo, N., Tanaka, A., Nakahara, T., Nagao, M., et al. (2019) · The Journal of Dermatology · doi:10.1111/1346-8138.15090 · Cited by 131
The Human Microbiota and Asthma
Heul, A. V., Planer, J. D., & Kau, A. L. (2018) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-018-8719-7 · Cited by 131
Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial
Simpson, M. R., Dotterud, C. K., Storrø, O., Johnsen, R., & Øien, T. (2015) · BMC Dermatology · doi:10.1186/s12895-015-0030-1 · Cited by 124
“Subsequently, probiotics have been investigated in the prevention and treatment of allergy related diseases [3–8], with the strongest evidence emerging for the primary prevention of atopic dermatitis [3–5].”
Guidance on the use of probiotics in clinical practice in children with selected clinical conditions and in specific vulnerable groups
Hojsak, I., Fabiano, V., Pop, T. L., Goulet, O., Zuccotti, G., Cokugras, F. C., Pettoello‐Mantovani, M., & Kolaček, S. (2018) · Acta Paediatrica · doi:10.1111/apa.14270 · Cited by 123
“Current recommendations The World Allergy Organization recommends the use of probiotics (i) in pregnant women who are carrying a child with a high risk of allergy, (ii) in breastfeeding women when the infant faces a high risk of allergy and (iii) in infants with atopic predisposition (34).”
Background
Vitamin D and Bronchial Asthma: An Overview of Data From the Past 5 Years
Hall, S. C., & Agrawal, D. K. (2017) · Clinical Therapeutics · doi:10.1016/j.clinthera.2017.04.002 · Cited by 122
Immunomodulation by Human Milk Oligosaccharides: The Potential Role in Prevention of Allergic Diseases
Zuurveld, M., van Witzenburg, N. P., Garssen, J., Folkerts, G., Stahl, B., Land, B. V., & Willemsen, L. E. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00801 · Cited by 126
A compromised developmental trajectory of the infant gut microbiome and metabolome in atopic eczema
Ta, L. D. H., Chan, J. C. Y., Yap, G. C., Purbojati, R. W., Drautz‐Moses, D. I., Michelle, K. Y., Tay, C. J. X., Huang, C., Kioh, D. Y. Q., Woon, J. Y., et al. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1801964 · Cited by 123
“Current evidence supports breastfeeding, and when not possible formula supplemented with prebiotics and/or probiotics as a nutritional solution may prevent the primary development of eczema by supporting a healthy gut microbiome.(39,40,41) Studies on the use of prebiotics to specifically support the colonization and e…”
BackgroundSelf-citation
Prebiotics for the prevention of allergies: A systematic review and meta‐analysis of randomized controlled trials
Cuello‐García, C. A., Fiocchi, A. G., Pawankar, R., Yepes-Núñez, J. J., Morgano, G. P., Zhang, Y., Agarwal, A., Gandhi, S., Terracciano, L., Schünemann, H. J., et al. (2017) · Clinical & Experimental Allergy · doi:10.1111/cea.13042 · Cited by 116
Self-citation
Probiotics for Prevention of Atopy and Food Hypersensitivity in Early Childhood
Zhang, G., Hu, H.-J., Liu, C., Zhang, Q., Shakya, S., & Li, Z. (2016) · Medicine · doi:10.1097/md.0000000000002562 · Cited by 113
“and based on very low quality evidence, with no specific recommendation regarding strains, dose, treatment duration, etc.(49) Hence, more work still needs to be done in this field.”
Background
Vitamin D and Microbiota: Is There a Link with Allergies?
Murdaca, G., Gerosa, A., Paladin, F., Petrocchi, L., Banchero, S., & Gangemi, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084288 · Cited by 121
Allergic Patients with Long-Term Asthma Display Low Levels of Bifidobacterium adolescentis
Hevia, A., Milani, C., López, P., Donado, C. D., Cuervo, A., González, S., Suárez, A., Turroni, F., Gueimonde, M., Ventura, M., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147809 · Cited by 109
The Maternal Diet, Gut Bacteria, and Bacterial Metabolites during Pregnancy Influence Offspring Asthma
Gray, L. E. K., O’Hely, M., Ranganathan, S., Sly, P. D., & Vuillermin, P. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00365 · Cited by 110
The Good, the Bad, and the Ugly of Pregnancy Nutrients and Developmental Programming of Adult Disease
Hsu, C., & Tain, Y. (2019) · Nutrients · doi:10.3390/nu11040894 · Cited by 108
Efficacy of Bifidobacterium longum alone or in multi-strain probiotic formulations during early life and beyond
Mills, S., Yang, B. K., Smith, G., Stanton, C., & Ross, R. P. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2186098 · Cited by 113
Mechanisms by Which Atopic Dermatitis Predisposes to Food Allergy and the Atopic March
Tham, E. H., & Leung, D. Y. M. (2018) · Allergy Asthma and Immunology Research · doi:10.4168/aair.2019.11.1.4 · Cited by 107
The Effectiveness of Probiotic Lactobacillus rhamnosus and Lactobacillus casei Strains in Children with Atopic Dermatitis and Cow’s Milk Protein Allergy: A Multicenter, Randomized, Double Blind, Placebo Controlled Study
Cukrowská, B., Ceregra, A., Maciorkowska, E., Surowska, B., Zegadło-Mylik, M. A., Konopka, E., Trojanowska, I., Zakrzewska, M., Bierła, J. B., Zakrzewski, M., et al. (2021) · Nutrients · doi:10.3390/nu13041169 · Cited by 106
Probiotics in Pediatrics. A Review and Practical Guide
Depoorter, L., & Vandenplas, Y. (2021) · Nutrients · doi:10.3390/nu13072176 · Cited by 112
IgE-mediated food allergy
Waserman, S., Bégin, P., & Watson, W. (2018) · Allergy, Asthma & Clinical Immunology · doi:10.1186/s13223-018-0284-3 · Cited by 64
Self-citation
The Australasian Society of Clinical Immunology and Allergy infant feeding for allergy prevention guidelines
Joshi, P., Smith, J., Vale, S., & Campbell, D. E. (2019) · The Medical Journal of Australia · doi:10.5694/mja2.12102 · Cited by 102
Maternal and Perinatal Factors Associated with the Human Milk Microbiome
Demmelmair, H., Jiménez, E., Collado, M. C., Salminen, S., & McGuire, M. K. (2020) · Current Developments in Nutrition · doi:10.1093/cdn/nzaa027 · Cited by 100
“Considering that it took the World Allergy Organization several years to generate position papers on the effectiveness of pre-and probiotics for allergy prevention in children (125, 126), slow decision-making processes in politics and legislation are not surprising.”
Background
Prevention and Management of Cow’s Milk Allergy in Non-Exclusively Breastfed Infants
Vandenplas, Y. (2017) · Nutrients · doi:10.3390/nu9070731 · Cited by 98
“The WAO guideline panel suggests: (i) using probiotics in pregnant women at high risk for having an allergic child; (ii) using probiotics in women who breastfeed infants at high risk of developing allergy; and (iii) using probiotics in infants at high risk of developing allergy [83].”
Method
Maternal microbe-specific modulation of the offspring microbiome and development during pregnancy and lactation
Tian, M., Li, Q., Zheng, T., Yang, S., Chen, F., Guan, W., & Zhang, S. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2206505 · Cited by 101
“The World Allergy Organization (WAO) guideline panel suggests the use of probiotics in pregnant and breasting women with children at high risk for allergies.(152) This recommendation could efficiently prevent the development of atopic eczema during childhood.”
Background
Bugging allergy; role of pre-, pro- and synbiotics in allergy prevention
West, C. E., Dzidic, M., Prescott, S. L., & Jenmalm, M. C. (2017) · Allergology International · doi:10.1016/j.alit.2017.08.001 · Cited by 97
Self-citation
Nutritional Issues in Food Allergy
Skypala, I. J., & McKenzie, R. (2018) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-018-8688-x · Cited by 94
“ferring a health benefit^, whereas probiotics are living microorganisms that have been proposed as immune-modulators of the allergic response [27, 28].”
Background
Preparation of Ca-alginate-whey protein isolate microcapsules for protection and delivery of L. bulgaricus and L. paracasei
Han, C., Xiao, Y., Liu, E., Su, Z., Meng, X., & Liu, B. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.07.247 · Cited by 94
The Role of Prebiotics and Probiotics in Prevention of Allergic Diseases in Infants
Sestito, S., D’Auria, E., Baldassarre, M. E., Salvatore, S., Tallarico, V., Stefanelli, E., Tarsitano, F., Concolino, D., & Pensabene, L. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.583946 · Cited by 96
Emerging evidence of the role of gut microbiota in the development of allergic diseases
Sjödin, K. S., Vidman, L., Rydén, P., & West, C. E. (2016) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000277 · Cited by 91
“The 2015 guidelines from the World Allergy Organization now declare that ‘there is a likely net benefit from using probiotics resulting primarily from prevention of eczema’ in infants at high risk of allergic disease [27], but in concordance with other expert organizations no advice on specific probiotic regimens is g…”
Background
Reviewing the evidence on breast milk composition and immunological outcomes
Boix-Amorós, A., Collado, M. C., Land, B. V., Calvert, A., Doaré, K. L., Garssen, J., Hanna, H., Khaleva, E., Peroni, D. G., Geddes, D. T., et al. (2019) · Nutrition Reviews · doi:10.1093/nutrit/nuz019 · Cited by 100
Towards Risk‐Free Trustworthy Artificial Intelligence: Significance and Requirements
Alzubaidi, L., Al-Sabaawi, A., Bai, J., Dukhan, A., Alkenani, A. H., Al‐Asadi, A., Alwzwazy, H. A., Manoufali, M., Fadhel, M. A., Albahri, A. S., et al. (2023) · International Journal of Intelligent Systems · doi:10.1155/2023/4459198 · Cited by 116
Prebiotics: Mechanisms and Preventive Effects in Allergy
Brosseau, C., Selle, A., Palmer, D. J., Prescott, S. L., Barbarot, S., & Bodinier, M. (2019) · Nutrients · doi:10.3390/nu11081841 · Cited by 100
Self-citation
Skin Care and Synbiotics for Prevention of Atopic Dermatitis or Food Allergy in Newborn Infants: A 2 × 2 Factorial, Randomized, Non-Treatment Controlled Trial
Dissanayake, E., Tani, Y., Nagai, K., Sahara, M., Mitsuishi, C., Togawa, Y., Suzuki, Y., Nakano, T., Yamaide, F., Ohno, H., et al. (2019) · International Archives of Allergy and Immunology · doi:10.1159/000501636 · Cited by 86
The Beneficial Effect of Farm Milk Consumption on Asthma, Allergies, and Infections: From Meta-Analysis of Evidence to Clinical Trial
Brick, T., Hettinga, K. A., Kirchner, B., Pfaffl, M. W., & Ege, M. J. (2019) · The Journal of Allergy and Clinical Immunology In Practice · doi:10.1016/j.jaip.2019.11.017 · Cited by 86
Probiotic Supplementation during the Perinatal and Infant Period: Effects on gut Dysbiosis and Disease
Navarro‐Tapia, E., Sebastiani, G., Sailer, S., Almeida-Toledano, L., Serra-Delgado, M., García‐Algar, Ó., & Andreu-Férnández, V. (2020) · Nutrients · doi:10.3390/nu12082243 · Cited by 86
Bacterial Metabolites: A Link between Gut Microbiota and Dermatological Diseases
Stec, A., Sikora, M., Maciejewska, M., Paralusz-Stec, K., Michalska, M. N., Sikorska, E., & Rudnicka, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043494 · Cited by 89
The microbiome in asthma
Kozik, A. J., & Huang, Y. J. (2018) · Annals of Allergy Asthma & Immunology · doi:10.1016/j.anai.2018.12.005 · Cited by 83
Probiotics as treatment for food allergies among pediatric patients: a meta-analysis
Tan‐Lim, C. S. C., & Esteban‐Ipac, N. A. R. (2018) · World Allergy Organization Journal · doi:10.1186/s40413-018-0204-5 · Cited by 80
“Probiotic use among infants at high risk of allergic disease was conditionally recommended due to its net benefit of preventing eczema; however this had very low quality of evidence [16].”
Background
Probiotics as a Potential Immunomodulating Pharmabiotics in Allergic Diseases: Current Status and Future Prospects
Sharma, G., & Im, S. (2018) · Allergy Asthma and Immunology Research · doi:10.4168/aair.2018.10.6.575 · Cited by 85
The Role of Probiotics in Preventing Allergic Disease
Wang, H. T., Anvari, S., & Anagnostou, A. (2019) · Children · doi:10.3390/children6020024 · Cited by 79
Probiotics in Asthma and Allergy Prevention
Mennini, M., Dahdah, L., Artesani, M. C., Fiocchi, A. G., & Martelli, A. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00165 · Cited by 79
Self-citation
Exploring the Science behind Bifidobacterium breve M-16V in Infant Health
Wong, C. B., Iwabuchi, N., & Xiao, J. (2019) · Nutrients · doi:10.3390/nu11081724 · Cited by 78
“Collectively, these findings are cautiously promising with respect to the use of probiotics for the primary prevention of eczema in pregnant mothers of infants at high risk for developing allergy and in high-risk infants, as recommended in recent guidelines from the World Allergy Organization [115].”
The Probiotics in Pregnancy Study (PiP Study): rationale and design of a double-blind randomised controlled trial to improve maternal health during pregnancy and prevent infant eczema and allergy
Barthow, C. A., Wickens, K. L., Stanley, T., Mitchell, E. A., Maude, R., Abels, P., Purdie, G., Murphy, R., STONE, P. R., Kang, J., et al. (2016) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-016-0923-y · Cited by 79
“A recent 2015 World Allergy Organisation guideline has for the first time suggested that pregnant women whose infants are at high risk for allergy should take probiotics; however this recommendation is recorded as conditional and based on very low quality evidence [80].”
Background
Food Allergy: Our Evolving Understanding of Its Pathogenesis, Prevention, and Treatment
Iweala, O. I., & Burks, A. W. (2016) · Current Allergy and Asthma Reports · doi:10.1007/s11882-016-0616-7 · Cited by 77
Pre‐ and probiotics for allergy prevention: time to revisit recommendations?
Forsberg, A., West, C. E., Prescott, S. L., & Jenmalm, M. C. (2016) · Clinical & Experimental Allergy · doi:10.1111/cea.12838 · Cited by 79
Self-citation
Probiotics in late infancy reduce the incidence of eczema: A randomized controlled trial
Schmidt, R. M., Laursen, R. P., Bruun, S., Larnkjær, A., Mølgaard, C., Michaelsen, K. F., & Høst, A. (2019) · Pediatric Allergy and Immunology · doi:10.1111/pai.13018 · Cited by 78
“Due to the beneficial effects on the development of eczema, The World Allergy Organization 81 guideline panel suggested in 2015 to use probiotics in pregnant women at high risk of having an 82 allergic child; women, who breastfeed infants a t high risk of developing allergy; and infants at high 83 risk of developing a…”
Background
Prebiotics and probiotics in atopic dermatitis (Review)
Rusu, E., Enache, G., Cursaru, R., Alexescu, A., Radu, R., Onila, O., Cavallioti, T., Rusu, F., Posea, M., Jinga, M., et al. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7678 · Cited by 77
The role of microbiota and enteroendocrine cells in maintaining homeostasis in the human digestive tract
Woźniak, D., Cichy, W., Przysławski, J., & Drzymała-Czyż, S. (2021) · Advances in Medical Sciences · doi:10.1016/j.advms.2021.05.003 · Cited by 80
Probiotics for gastrointestinal disorders: Proposed recommendations for children of the Asia-Pacific region
Cameron, D. J. S., Hock, Q. S., Kadim, M., Mohan, N., Ryoo, E., Sandhu, B., Yamashiro, Y., Chen, J., Hoekstra, H., & Guarino, A. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i45.7952 · Cited by 78
Microbial Dysbiosis Tunes the Immune Response Towards Allergic Disease Outcomes
Augustine, T., Kumar, M., Khodor, S. A., & van Panhuys, N. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-022-08939-9 · Cited by 76
Term Infant Formulas Influencing Gut Microbiota: An Overview
Fabiano, V., Indrio, F., Verduci, E., Calcaterra, V., Pop, T. L., Mari, A., Zuccotti, G., Cokugras, F. C., Pettoello‐Mantovani, M., & Goulet, O. (2021) · Nutrients · doi:10.3390/nu13124200 · Cited by 78
The Significance of the Enteric Microbiome on the Development of Childhood Disease: A Review of Prebiotic and Probiotic Therapies in Disorders of Childhood
Slattery, J. M., MacFabe, D. F., & Frye, R. E. (2016) · Clinical Medicine Insights Pediatrics · doi:10.4137/cmped.s38338 · Cited by 72
Prebiotics in the Infant Microbiome: The Past, Present, and Future
Miqdady, M. S., Mistarihi, J. A., Azaz, A., & Rawat, D. J. (2020) · Pediatric Gastroenterology Hepatology & Nutrition · doi:10.5223/pghn.2020.23.1.1 · Cited by 74
Cow’s Milk Allergy: Immunomodulation by Dietary Intervention
D’Auria, E., Salvatore, S., Pozzi, E., Mantegazza, C., Sartorio, M. U. A., Pensabene, L., Baldassarre, M. E., Agosti, M., Vandenplas, Y., & Zuccotti, G. (2019) · Nutrients · doi:10.3390/nu11061399 · Cited by 70
“However, the WAO guideline panel recognizes that the recommendations of both probiotics and prebiotics are conditional and based on very low quality evidence.”
Background
Influences on allergic mechanisms through gut, lung, and skin microbiome exposures
Kemter, A. M., & Nagler‐Anderson, C. (2019) · Journal of Clinical Investigation · doi:10.1172/jci124610 · Cited by 78
“The available data suggest that the efficacy of traditional probiotics is limited to the prevention of eczema in high-risk infants (156, 167, 168).”
Background
Human milk microbiome: From actual knowledge to future perspective
Selma‐Royo, M., Calvo‐Lerma, J., Cortés-Macías, E., & Collado, M. C. (2021) · Seminars in Perinatology · doi:10.1016/j.semperi.2021.151450 · Cited by 76
Strategies and Future Opportunities for the Prevention, Diagnosis, and Management of Cow Milk Allergy
Zepeda-Ortega, B., Goh, A., Xepapadaki, P. V., Sprikkelman, A. B., Nicolaou, N. C., Hernández, R. E. H., Latiff, A. H. A., Yat, M. T., Diab, M., Hussaini, B. A., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.608372 · Cited by 69
Current Use of Probiotics and Prebiotics in Allergy
Fiocchi, A. G., Cabana, M. D., & Mennini, M. (2022) · The Journal of Allergy and Clinical Immunology In Practice · doi:10.1016/j.jaip.2022.06.038 · Cited by 68
Self-citation
Manipulating Microbiota to Treat Atopic Dermatitis: Functions and Therapies
Alam, J., Xie, L., Yap, Y. A., Marques, F. Z., & Robert, R. (2022) · Pathogens · doi:10.3390/pathogens11060642 · Cited by 71
Allergy prevention by breastfeeding: possible mechanisms and evidence from human cohorts
Munblit, D., & Verhasselt, V. (2016) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000303 · Cited by 73
Food allergy and atopic dermatitis: Prediction, progression, and prevention
Mastrorilli, C., Caffarelli, C., & Hoffmann‐Sommergruber, K. (2017) · Pediatric Allergy and Immunology · doi:10.1111/pai.12831 · Cited by 66
A Comprehensive Review on Natural Bioactive Compounds and Probiotics as Potential Therapeutics in Food Allergy Treatment
Pratap, K., Taki, A. C., Johnston, E. B., Lopata, A. L., & Kamath, S. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00996 · Cited by 66
Epicutaneous sensitization to food allergens in atopic dermatitis: What do we know?
Tham, E. H., Rajakulendran, M., Lee, B. W., & Bever, H. P. S. V. (2019) · Pediatric Allergy and Immunology · doi:10.1111/pai.13127 · Cited by 67
Self-citation
Food Allergy Prevention and Treatment by Targeted Nutrition
Heine, R. G. (2018) · Annals of Nutrition and Metabolism · doi:10.1159/000487380 · Cited by 64
Awareness, Knowledge, and Interest about Prebiotics—A Study among Romanian Consumers
Precup, G., Pocol, C. B., Teleky, B., & Vodnar, D. C. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19031208 · Cited by 71
The role of the commensal microbiota in the regulation of tolerance to dietary allergens
Canani, R. B., Gilbert, J. A., & Nagler‐Anderson, C. (2015) · Current Opinion in Allergy and Clinical Immunology · doi:10.1097/aci.0000000000000157 · Cited by 63
“Recently published guidelines for atopic disease prevention from the World Allergy Organization concluded that there is a likely net benefit in using probiotics for eczema prevention [35].”
Background
Probiotics for treatment and primary prevention of allergic diseases and asthma: looking back and moving forward
West, C. E., Jenmalm, M. C., Kozyrskyj, A. L., & Prescott, S. L. (2016) · Expert Review of Clinical Immunology · doi:10.1586/1744666x.2016.1147955 · Cited by 61
“In 2015, the WAO launched guidelines on the use of probiotics as a preventive strategy to reduce allergic diseases [96].”
BackgroundMethodSelf-citation
Long-term safety assessment in children who received hydrolyzed protein formulas with Lactobacillus rhamnosus GG: a 5-year follow-up
Scalabrin, D., Harris, C. L., Johnston, W., & Berseth, C. L. (2016) · European Journal of Pediatrics · doi:10.1007/s00431-016-2825-4 · Cited by 62
“Although safety issues associated with the use of live probiotic bacteria are rare and have been reported only in immunocompromised or seriously ill individuals, there are still safety concerns associated with the use of live probiotic bacteria [33, 34].”
Background
Probiotics: a proactive approach to health. A symposium report
Thomas, L. V., Suzuki, K., & Zhao, J. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114515004043 · Cited by 61
“∙ Prevention of allergic disease: in 2015, the World Allergy Organization published new evidence-based guidelines relating to probiotic use((57)).”
Background

World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Prebiotics
Cuello‐García, C. A., Fiocchi, A. G., Pawankar, R., Yepes-Núñez, J. J., Morgano, G. P., Zhang, Y., Ahn, K., Al‐Hammadi, S., Agarwal, A., Gandhi, S., et al. (2016) · World Allergy Organization Journal · doi:10.1186/s40413-016-0102-7 · Cited by 155
Self-citation
A clinical reading on “World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics”
Ricci, G., Cipriani, F., Cuello‐García, C. A., Brożek, J., Fiocchi, A. G., Pawankar, R., Yepes-Núñez, J. J., Terracciano, L., Gandhi, S., Agarwal, A., et al. (2016) · World Allergy Organization Journal · doi:10.1186/s40413-016-0101-8 · Cited by 19
Self-citation
LP-13 Integrating New Approach Methodologies in food safety assessments. Ongoing EFSA Case Studies
Cattaneo, I., Astuto, M. C., Liem, D., & Tarazona, J. V. (2022) · Toxicology Letters · doi:10.1016/j.toxlet.2022.07.757 · Cited by 1
Probiotics for the prevention of allergy: A systematic review and meta-analysis of randomized controlled trials
Cuello-Garcia, C. A., Brożek, J. L., Fiocchi, A., Pawankar, R., Yepes-Nuñez, J. J., Terracciano, L., Gandhi, S., Agarwal, A., Zhang, Y., & Schünemann, H. J. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.04.031 · Cited by 383
Self-citation
Probiotics for Irritable Bowel Syndrome: Clinical Data in Children.
Giannetti, E., & Staiano, A. (2016) · PubMed · doi:10.1097/mpg.0000000000001220 · Cited by 23
Self-citation

Authors: Fiocchi, A., Pawankar, R., Cuello-Garcia, C., Ahn, K., Al-Hammadi, S., Agarwal, A., Beyer, K., Burks, W., Canonica, G. W., Ebisawa, M., Gandhi, S., Kamenwa, R., Lee, B. W., Li, H., Prescott, S., Riva, J. J., Rosenwasser, L., Sampson, H., Spigler, M., Terracciano, L., Vereda-Ortiz, A., Waserman, S., Yepes-Nuñez, J. J., Brożek, J. L., & Schünemann, H. J.
Affiliations: Bambino Gesù Children's Hospital (IT)
Nippon Medical School (JP)
Samsung Medical Center (KR)
University of Toronto (CA)
Stiftung Charité (DE)
University of North Carolina at Chapel Hill (US)
Ospedale Policlinico San Martino (IT)
National Sagamihara Hospital (JP)
Aga Khan University Hospital Nairobi (KE)
National University of Singapore (SG)
Children's Hospital of Chongqing Medical University (CN)
The Kids Research Institute Australia (AU)
McMaster University (CA)
Children's Mercy Hospital (US)
Icahn School of Medicine at Mount Sinai (US)
Food Allergy Research and Education (US)
University of Milan (IT)
Hospital Infantil Universitario Niño Jesús (ES)
Corresponding author: Fiocchi, Alessandro
Pawankar, Ruby
Brożek, Jan L
ORCID: Fiocchi, Alessandro
Pawankar, Ruby
Ahn, Kangmo
Agarwal, Arnav
Beyer, Kirsten
Canonica, Giorgio W
Ebisawa, Motohiro
Kamenwa, Rose
Lee, Bee Wah
Prescott, Susan
Riva, John J
Rosenwasser, Lanny
Sampson, Hugh
Terracciano, Luigi
Waserman, Susan
Brożek, Jan L
Schünemann, Holger J
Venue: World Allergy Organization Journal
Publisher: Elsevier BV
Published: 2015
Volume: 8
Issue: 1
Pages: 4
ISSN: 1939-4551 (ISSN-L)
DOI: 10.1186/s40413-015-0055-2
PMC: PMC4307749
OpenAlex: W2141887889
Cited by: 473
References: 119
Citations by year: 2026: 6 · 2025: 23 · 2024: 40 · 2023: 43 · 2022: 36 · 2021: 45 · 2020: 54 · 2019: 48 · 2018: 47 · 2017: 45 · 2016: 56 · 2015: 29
FWCI: 78.90
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by-nc-nd/4.0/ (vor, 1583 d)
www.springer.com/tdm (unspecified)
Locations: World Allergy Organization Journal (publishedVersion, cc-by-nc-nd)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Institutional Repository University of Antioquia (University of Antioquia) (publishedVersion, cc-by-nc-nd)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
TSpace (University of Toronto) (submittedVersion)
eCommons - AKU (Aga Khan University) (submittedVersion)
UWA Profiles and Research Repository (UWA) (submittedVersion, other-oa)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
UNC Libraries
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Health Sciences › Medicine › Immunology and Allergy › Food Allergy and Anaphylaxis Research
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Asthma and respiratory diseases
Keywords: probiotics, allergy prevention, infants, eczema prevention, gut microbiota, probiotic supplementation, pregnancy, breastfeeding, high-risk infants, immunomodulation

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

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