Efficacy and Safety of Oral Probiotics in Children with Allergic Rhinitis: A Review

The prevalence of allergic rhinitis is rising, and it is impacting children’s growth and quality of life. To uncover unconventional treatment modalities, research was carried out to clarify the significance of novel components in the pathophysiology of allergic rhinitis. One of these elements was gut microbiota, which plays a crucial role in the development and evolution of allergic disorders. Specifically, dysbiosis, defined as impaired microbiota composition, characterizes allergic disorders. In light of this concept, probiotics (beneficial bacteria) may restore gut dysbiosis, rebalance the immune response, and indirectly influence the clinical course of allergic diseases. In this article, we discussed the role of the gut–lung axis in children and reported on new findings. We also reviewed the most relevant studies about probiotics in patients with allergic rhinitis.

[1]  T. Yeh,et al.  Recent Updates of Immunotherapy for Allergic Rhinitis in Children , 2023, Current Otorhinolaryngology Reports.

[2]  Nilgün Özdemir,et al.  Multifunctional potentials of lactic acid bacterial isolates from Turkish traditional fermented foods. , 2023, Letters in applied microbiology.

[3]  M. Caminati,et al.  Diagnosis and Management of Allergic Rhinitis in Asthmatic Children , 2023, Journal of asthma and allergy.

[4]  Sokho Kim,et al.  Effects of yogurt containing probiotics on respiratory virus infections: Influenza H1N1 and SARS-CoV-2 , 2023, Journal of Dairy Science.

[5]  A. Zicari,et al.  An Overview on the Primary Factors That Contribute to Non-Allergic Asthma in Children , 2022, Journal of clinical medicine.

[6]  P. Liu,et al.  Research Advances in the Treatment of Allergic Rhinitis by Probiotics , 2022, Journal of asthma and allergy.

[7]  J. Bousquet,et al.  Non-allergic Rhinitis, Allergic Rhinitis and Immunotherapy: Advances in the Last Decade. , 2022, The journal of allergy and clinical immunology. In practice.

[8]  G. Botsaris,et al.  Beneficial Effects of Yoghurts and Probiotic Fermented Milks and Their Functional Food Potential , 2022, Foods.

[9]  G. Ciprandi,et al.  Mometasone furoate nasal spray in Italian children with seasonal allergic rhinitis: a comprehensive assessment. , 2022, Allergologia et immunopathologia.

[10]  G. Ciprandi,et al.  (R)Evolution in Allergic Rhinitis Add-On Therapy: From Probiotics to Postbiotics and Parabiotics , 2022, Journal of clinical medicine.

[11]  Ż. Kimber-Trojnar,et al.  Effects of Probiotic Supplementation during Pregnancy on the Future Maternal Risk of Metabolic Syndrome , 2022, International journal of molecular sciences.

[12]  S. Peng,et al.  The Efficacy and Safety of Probiotics for Allergic Rhinitis: A Systematic Review and Meta-Analysis , 2022, Frontiers in Immunology.

[13]  H. Zhang,et al.  Efficacy and Safety of Lactobacillus reuteri CCFM1040 in Allergic Rhinitis and Asthma: A Randomized, Placebo-Controlled Trial , 2022, Frontiers in Nutrition.

[14]  Shohei Akagawa,et al.  Gut microbiota and allergic diseases in children. , 2022, Allergology international : official journal of the Japanese Society of Allergology.

[15]  L. Mcfarland,et al.  Effects of Probiotics on Allergic Rhinitis: A Systematic Review and Meta-Analysis of Randomized Clinical Trials , 2022, American journal of rhinology & allergy.

[16]  Jiai Yan,et al.  Roles of the gut microbiota in severe SARS-CoV-2 infection , 2022, Cytokine & Growth Factor Reviews.

[17]  A. Lorentz,et al.  Probiotic Potential of Lactobacillus Species in Allergic Rhinitis , 2021, International Archives of Allergy and Immunology.

[18]  K. Kaneko,et al.  Decreased butyric acid‐producing bacteria in gut microbiota of children with egg allergy , 2021, Allergy.

[19]  G. L. D. de Oliveira,et al.  Microbiota Modulation of the Gut-Lung Axis in COVID-19 , 2021, Frontiers in Immunology.

[20]  T. Kabuki,et al.  Lactobacillus helveticus SBT2171 Alleviates Perennial Allergic Rhinitis in Japanese Adults by Suppressing Eosinophils: A Randomized, Double-Blind, Placebo-Controlled Study , 2020, Nutrients.

[21]  Wei Chen,et al.  Lactobacillus reuteri CCFM1072 and CCFM1040 with the role of Treg cells regulation alleviate airway inflammation through modulating gut microbiota in allergic asthma mice , 2020 .

[22]  A. Licari,et al.  Allergen immunotherapy in children and adolescents with respiratory diseases , 2020, Acta bio-medica : Atenei Parmensis.

[23]  Wenlong Liu,et al.  Compliance, efficacy, and safety of subcutaneous and sublingual immunotherapy in children with allergic rhinitis , 2020, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[24]  A. Licari,et al.  Allergen Immunotherapy in Pediatric Asthma: A Pragmatic Point of View , 2020, Children.

[25]  T. Dinan,et al.  Recipe for a Healthy Gut: Intake of Unpasteurised Milk Is Associated with Increased Lactobacillus Abundance in the Human Gut Microbiome , 2020, Nutrients.

[26]  Wei Chen,et al.  Lactobacillus reuteri attenuated allergic inflammation induced by HDM in the mouse and modulated gut microbes , 2020, PloS one.

[27]  A. Tam,et al.  Gastrointestinal Manifestations of SARS-CoV-2 Infection and Virus Load in Fecal Samples From a Hong Kong Cohort: Systematic Review and Meta-analysis , 2020, Gastroenterology.

[28]  H. Shan,et al.  Gastrointestinal symptoms of 95 cases with SARS-CoV-2 infection , 2020, Gut.

[29]  L. Cox Approach to Patients with Allergic Rhinitis: Testing and Treatment. , 2020, The Medical clinics of North America.

[30]  M. Ahmed,et al.  Efficacy of probiotic in perennial allergic rhinitis under five year children: A randomized controlled trial , 2019, Pakistan journal of medical sciences.

[31]  A. Shetty,et al.  BACILLUS CLAUSII SEPTICEMIA IN A PEDIATRIC PATIENT AFTER TREATMENT WITH PROBIOTICS. , 2019, The Pediatric infectious disease journal.

[32]  A. Terpou,et al.  Probiotics in Food Systems: Significance and Emerging Strategies Towards Improved Viability and Delivery of Enhanced Beneficial Value , 2019, Nutrients.

[33]  Xizi Du,et al.  Efficacy of probiotic supplementary therapy for asthma, allergic rhinitis, and wheeze: a meta-analysis of randomized controlled trials. , 2019, Allergy and asthma proceedings.

[34]  N. Matsumoto,et al.  Anti-allergic effect of Lactobacillus helveticus SBT2171 on murine model of pollen allergy , 2019, Functional Foods in Health and Disease.

[35]  M. Han,et al.  Bifidobacterium longum IM55 and Lactobacillus plantarum IM76 alleviate allergic rhinitis in mice by restoring Th2/Treg imbalance and gut microbiota disturbance. , 2019, Beneficial microbes.

[36]  C. Akdis,et al.  High levels of butyrate and propionate in early life are associated with protection against atopy , 2018, Allergy.

[37]  M. Hashemi,et al.  The immunomodulatory role of probiotics in allergy therapy , 2018, Journal of cellular physiology.

[38]  D. Price,et al.  Next-generation Allergic Rhinitis and Its Impact on Asthma (ARIA) guidelines for allergic rhinitis based on Grading of Recommendations Assessment, Development and Evaluation (GRADE) and real-world evidence. , 2019, The Journal of allergy and clinical immunology.

[39]  L. Iughetti,et al.  Changes of intestinal microbiota in early life , 2018, The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians.

[40]  C. Bachert,et al.  Immunomodulatory effect of Bifidobacterium breve on experimental allergic rhinitis in BALB/c mice , 2018, Experimental and therapeutic medicine.

[41]  F. Di Pierro,et al.  Use of a probiotic mixture containing Bifidobacterium animalis subsp. lactis BB12 and Enterococcus faecium L3 in atopic children. , 2018, Minerva pediatrica.

[42]  T. Chun,et al.  Oral administration of Lactobacillus plantarum CJLP133 and CJLP243 alleviates birch pollen‐induced allergic rhinitis in mice , 2018, Journal of applied microbiology.

[43]  P. Matricardi,et al.  Diagnostic relevance of IgE sensitization profiles to eight recombinant Phleum pratense molecules , 2018, Allergy.

[44]  A. Sheikh,et al.  国际过敏与鼻科学共识声明 : 变应性鼻炎 , 2018 .

[45]  C. Su,et al.  [Clinical observation of saccharomyces boulardii combined with cetirizine hydrochloride in children allergic rhinitis]. , 2017, Lin chuang er bi yan hou tou jing wai ke za zhi = Journal of clinical otorhinolaryngology, head, and neck surgery.

[46]  M. Underwood,et al.  Prenatal and postnatal administration of prebiotics and probiotics. , 2017, Seminars in fetal & neonatal medicine.

[47]  J. Gordon,et al.  Lactobacillus reuteri induces gut intraepithelial CD4+CD8αα+ T cells , 2017, Science.

[48]  Hee Kang,et al.  Enterococcus faecium FC-K Derived from Kimchi Is a Probiotic Strain That Shows Anti-Allergic Activity. , 2017, Journal of microbiology and biotechnology.

[49]  M. Schloter,et al.  D‐tryptophan from probiotic bacteria influences the gut microbiome and allergic airway disease , 2017, The Journal of allergy and clinical immunology.

[50]  A. Pihlanto,et al.  Health benefits of fermented foods: microbiota and beyond. , 2017, Current opinion in biotechnology.

[51]  M. M. del Giudice,et al.  Bifidobacterium mixture (B longum BB536, B infantis M-63, B breve M-16V) treatment in children with seasonal allergic rhinitis and intermittent asthma , 2017, Italian Journal of Pediatrics.

[52]  S. Salminen,et al.  Long‐term safety and efficacy of perinatal probiotic intervention: Evidence from a follow‐up study of four randomized, double‐blind, placebo‐controlled trials , 2017, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[53]  O. Koren,et al.  The Pregnancy Microbiome. , 2017, Nestle Nutrition Institute workshop series.

[54]  N. Crum‐Cianflone,et al.  The potential risks of probiotics among HIV-infected persons: Bacteraemia due to Lactobacillus acidophilus and review of the literature , 2016, International journal of STD & AIDS.

[55]  J. Domínguez-Ortega,et al.  The Use of Probiotics in Respiratory Allergy , 2016 .

[56]  O. Koren,et al.  Antibiotic use during pregnancy: how bad is it? , 2016, BMC Medicine.

[57]  D. Bernstein,et al.  Allergic Rhinitis: Mechanisms and Treatment. , 2016, Immunology and allergy clinics of North America.

[58]  U. Sauer,et al.  The maternal microbiota drives early postnatal innate immune development , 2016, Science.

[59]  S. Mazmanian,et al.  Gut biogeography of the bacterial microbiota , 2015, Nature Reviews Microbiology.

[60]  Aly A. Khan,et al.  Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants , 2015, The ISME Journal.

[61]  C. A. De Castro,et al.  Oral administration of Lactobacillus paracasei NCC 2461 for the modulation of grass pollen allergic rhinitis: a randomized, placebo-controlled study during the pollen season , 2015, Clinical and Translational Allergy.

[62]  L. Morelli,et al.  Probiotics for prevention of atopic diseases in infants: systematic review and meta‐analysis , 2015, Allergy.

[63]  F. Rodenas,et al.  MACVIA‐ARIA Sentinel NetworK for allergic rhinitis (MASK‐rhinitis): the new generation guideline implementation , 2015, Allergy.

[64]  R. Johnsen,et al.  Perinatal probiotic supplementation in the prevention of allergy related disease: 6 year follow up of a randomised controlled trial , 2015, BMC Dermatology.

[65]  Kirsten Beyer,et al.  World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): Probiotics , 2015, The World Allergy Organization journal.

[66]  N. Waki,et al.  Effects of probiotic Lactobacillus brevis KB290 on incidence of influenza infection among schoolchildren: an open-label pilot study , 2014, Letters in applied microbiology.

[67]  J. Bellanti,et al.  United airway disease , 2014, Allergy and asthma proceedings.

[68]  L. Fu,et al.  Evaluation of the effect of Lactobacillus paracasei (HF.A00232) in children (6-13 years old) with perennial allergic rhinitis: a 12-week, double-blind, randomized, placebo-controlled study. , 2014, Pediatrics and neonatology.

[69]  J. Bousquet,et al.  Efficacy and safety of the probiotic Lactobacillus paracasei LP-33 in allergic rhinitis: a double-blind, randomized, placebo-controlled trial (GA2LEN Study) , 2014, European Journal of Clinical Nutrition.

[70]  F. Spertini,et al.  Comparison of two oral probiotic preparations in a randomized crossover trial highlights a potentially beneficial effect of Lactobacillus paracasei NCC2461 in patients with allergic rhinitis , 2014, Clinical and Translational Allergy.

[71]  O. Ruuskanen,et al.  Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: A randomized, placebo-controlled trial , 2013, Journal of Allergy and Clinical Immunology.

[72]  M. Nitert,et al.  Probiotics and Pregnancy , 2014, Current Diabetes Reports.

[73]  M. Longnecker,et al.  Probiotic milk consumption in pregnancy and infancy and subsequent childhood allergic diseases. , 2014, The Journal of allergy and clinical immunology.

[74]  A. De Luca,et al.  Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. , 2013, Immunity.

[75]  Elaheh Vahabnezhad,et al.  Lactobacillus bacteremia associated with probiotic use in a pediatric patient with ulcerative colitis. , 2013, Journal of clinical gastroenterology.

[76]  S. Wen,et al.  Effect of probiotics on allergic rhinitis in Df, Dp or dust-sensitive children: A randomized double blind controlled trial , 2013, Indian Pediatrics.

[77]  L. T. Angenent,et al.  Host Remodeling of the Gut Microbiome and Metabolic Changes during Pregnancy , 2012, Cell.

[78]  Aleksandar Milosavljevic,et al.  A Metagenomic Approach to Characterization of the Vaginal Microbiome Signature in Pregnancy , 2012, PloS one.

[79]  J. Bousquet,et al.  A novel intranasal therapy of azelastine with fluticasone for the treatment of allergic rhinitis. , 2012, The Journal of allergy and clinical immunology.

[80]  T. Shimada,et al.  Effects of lysed Enterococcus faecalis FK-23 on experimental allergic rhinitis in a murine model , 2012, Journal of biomedical research.

[81]  De-min Han,et al.  [Allergic rhinoconjunctivitis]. , 2012, Zhonghua er bi yan hou tou jing wai ke za zhi = Chinese journal of otorhinolaryngology head and neck surgery.

[82]  L. Perrone,et al.  Allergic Rhinitis and Quality of Life in Children , 2011, International journal of immunopathology and pharmacology.

[83]  F. Spertini,et al.  Effect of Lactobacillus paracasei ST11 on a nasal provocation test with grass pollen in allergic rhinitis , 2011, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[84]  J. Carlin,et al.  Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial , 2011, Allergy.

[85]  H. Ohno,et al.  Effects of Bifidobacterium bifidum G9-1 on Nasal Symptoms in a Guinea Pig Model of Experimental Allergic Rhinitis , 2010, Bioscience and microflora.

[86]  Ren-Long Jan,et al.  Randomized placebo‐controlled trial of lactobacillus on asthmatic children with allergic rhinitis , 2010, Pediatric pulmonology.

[87]  Holger J Schünemann,et al.  Allergic Rhinitis and its Impact on Asthma (ARIA) guidelines: 2010 revision. , 2010, The Journal of allergy and clinical immunology.

[88]  M. Takase,et al.  Effects of Bifidobacterium longum BB536 Administration on Influenza Infection, Influenza Vaccine Antibody Titer, and Cell-Mediated Immunity in the Elderly , 2010, Bioscience, biotechnology, and biochemistry.

[89]  P. Rutgeerts,et al.  Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease. , 2010, Journal of medical microbiology.

[90]  J. Xaus,et al.  A probiotic dairy product containing L. gasseri CECT5714 and L. coryniformis CECT5711 induces immunological changes in children suffering from allergy , 2009, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[91]  S. Salminen,et al.  Specific probiotics alleviate allergic rhinitis during the birch pollen season. , 2009, World journal of gastroenterology.

[92]  Harry J. Flint,et al.  Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. , 2009, FEMS microbiology letters.

[93]  M. Falagas,et al.  Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trials. , 2008, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[94]  J. Doré,et al.  Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients , 2008, Proceedings of the National Academy of Sciences.

[95]  F. He,et al.  Orally Administrated Lactobacillus gasseri TMC0356 and Lactobacillus GG Alleviated Nasal Blockage of Guinea Pig with Allergic Rhinitis , 2007, Microbiology and immunology.

[96]  G. Radaelli,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 , 2007, Pediatric Research.

[97]  S. Prescott,et al.  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. , 2007, The Journal of allergy and clinical immunology.

[98]  M. Tamura,et al.  Effects of Probiotics on Allergic Rhinitis Induced by Japanese Cedar Pollen: Randomized Double-Blind, Placebo-Controlled Clinical Trial , 2006, International Archives of Allergy and Immunology.

[99]  F. He,et al.  Inhibitory Effect of Lactobacillus gasseri TMC0356 and Lactobacillus GG on Enhanced Vascular Permeability of Nasal Mucosa in Experimental Allergic Rhinitis of Rats , 2006, Bioscience, biotechnology, and biochemistry.

[100]  N. Iwabuchi,et al.  Probiotics in the treatment of Japanese cedar pollinosis: a double‐blind placebo‐controlled trial , 2006, Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology.

[101]  J. Grainger,et al.  Montelukast in allergic rhinitis: a systematic review and meta‐analysis , 2006, Clinical otolaryngology : official journal of ENT-UK ; official journal of Netherlands Society for Oto-Rhino-Laryngology & Cervico-Facial Surgery.

[102]  J. Xaus,et al.  Dietary deprivation of fermented foods causes a fall in innate immune response. Lactic acid bacteria can counteract the immunological effect of this deprivation , 2006, Journal of Dairy Research.

[103]  S. Salminen,et al.  Preliminary Human Study for Possible Alteration of Serum Immunoglobulin E Production in Perennial Allergic Rhinitis with Fermented Milk Prepared with Lactobacillus gasseri TMC0356 , 2006, Microbiology and immunology.

[104]  J. Xaus,et al.  Oral administration of two probiotic strains, Lactobacillus gasseri CECT5714 and Lactobacillus coryniformis CECT5711, enhances the intestinal function of healthy adults. , 2006, International journal of food microbiology.

[105]  J. Xaus,et al.  The consumption of two new probiotic strains, Lactobacillus gasseri CECT 5714 and Lactobacillus coryniformis CECT 5711, boosts the immune system of healthy humans. , 2006, International microbiology : the official journal of the Spanish Society for Microbiology.

[106]  Ching‐Hsiang Hsu,et al.  The efficacy and safety of heat‐killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house‐dust mite , 2005, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[107]  O. Kajimoto,et al.  Clinical effects of Lactobacillus acidophilus strain L-92 on perennial allergic rhinitis: a double-blind, placebo-controlled study. , 2005, Journal of dairy science.

[108]  N. Yamamoto,et al.  Effect of Milk Fermented with Lactobacillus acidophilus Strain L-92 on Symptoms of Japanese Cedar Pollen Allergy: A Randomized Placebo-Controlled Trial , 2005, Bioscience, biotechnology, and biochemistry.

[109]  Hsiao-Chuan Lin,et al.  Treatment of perennial allergic rhinitis with lactic acid bacteria , 2004, Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology.

[110]  T. Haahtela,et al.  No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch‐pollen allergy: a placebo‐controlled double‐blind study , 2002, Allergy.

[111]  F. D. de Benedictis,et al.  Rhinitis, sinusitis and asthma: one linked airway disease. , 2001, Paediatric respiratory reviews.

[112]  S. Salminen,et al.  Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial , 2001, The Lancet.

[113]  S. Kohno,et al.  Comparison of cedar pollen-induced allergic rhinitis in passively and actively sensitized guinea pigs. , 2001, Japanese journal of pharmacology.

[114]  C. White,et al.  Comparison of exhaled nitric oxide to spirometry during emergency treatment of asthma exacerbations with glucocorticoids in children. , 1999, Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology.

[115]  E. Isolauri,et al.  Probiotics: a novel approach in the management of food allergy. , 1997, The Journal of allergy and clinical immunology.

[116]  J. D. de Vries,et al.  Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells , 1996, The Journal of experimental medicine.

[117]  D. Yates,et al.  Inhaled glucocorticoids decrease nitric oxide in exhaled air of asthmatic patients. , 1996, American journal of respiratory and critical care medicine.

[118]  G. Trinchieri,et al.  Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma- production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells , 1993, The Journal of experimental medicine.

[119]  A. B. Kay,et al.  Asthma and inflammation. , 1991, The Journal of allergy and clinical immunology.

[120]  J. H. Wells,et al.  A noninvasive technique for measurement of changes in specific airway resistance. , 1979, Journal of applied physiology: respiratory, environmental and exercise physiology.

[121]  R. Settipane,et al.  Allergic rhinitis , 2005, Rhinology and Anterior Skull Base Surgery.