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

Clinical and Translational Allergy

François Spertini²  Annick Mercenier³  Corinne Magliola³  Anurag Singh³  Julie Moulin³  Vincent Aubert²  Nathalie Barbier²  Jacqueline Wassenberg²  Rodrigo Bibiloni¹  Bernard Berger³  Régine Audran²  Sophie Nutten³  Yannick Perrin² 

[1] Current address: AgResearch Ltd, Food and Bio-based Products, Hamilton, New Zealand;Division of Immunology and Allergy, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland;Nestlé Research Centre, Lausanne, Switzerland

关键词: Grass pollen;    Clinical trial;    Lactobacillus paracasei;    Nasal provocation test;    Immunomodulation;    Allergic rhinitis;   

Others  :  794095
DOI  :  10.1186/2045-7022-4-1

 received in 2013-06-05, accepted in 2013-12-17,  发布年份 2014

【 摘 要 】

Background

There is promising but conflicting evidence to recommend the addition of probiotics to foods for prevention and treatment of allergy. Based on previous studies with fermented milk containing Lactobacillus paracasei NCC2461, we aimed to compare the effect of a powder form of the latter probiotic with the effect of a blend of Lactobacillus acidophilus ATCC SD5221 and Bifidobacterium lactis ATCC SD5219 in patients with allergic rhinitis.

Methods

A double-blind, randomized, cross-over study, involving 31 adults with allergic rhinitis to grass pollen, was performed outside the grass pollen season (registration number: NCT01233154). Subjects received each product for 4-weeks in two phases separated by a wash-out period of 6 to 8 weeks. A nasal provocation test was performed before and after each 4-week product intake period, and outcome parameters (objective and subjective clinical symptoms; immune parameters) were measured during and/or 24 hours after the test.

Results

Out of the 31 subject enrolled, 28 completed the study. While no effect was observed on nasal congestion (primary outcome), treatment with NCC2461 significantly decreased nasal pruritus (determined by VAS), and leukocytes in nasal fluid samples, enhanced IL-5, IL-13 and IL-10 production by peripheral blood mononuclear cells in an allergen specific manner and tended to decrease IL-5 secretion in nasal fluid, in contrast to treatment with the blend of L. acidophilus and B. lactis.

Conclusions

Despite short-term consumption, NCC2461 was able to reduce subjective nasal pruritus while not affecting nasal congestion in adults suffering from grass pollen allergic rhinitis. The associated decrease in nasal fluid leukocytes and IL-5 secretion, and the enhanced IL-10 secretion in an allergen specific manner may partly explain the decrease in nasal pruritus. However, somewhat unexpected systemic immune changes were also noted. These data support the study of NCC2461 consumption in a seasonal clinical trial to further demonstrate its potentially beneficial effect.

【 授权许可】

   
2014 Perrin et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kalliomaki M, Antoine JM, Herz U, Rijkers GT, Wells JM, Mercenier A: Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of allergic diseases by probiotics. J Nutr 2010, 140:713-721.
• [2]Laitinen K, Isolauri E: Management of food allergy: vitamins, fatty acids or probiotics? Eur J Gastroenterol Hepatol 2005, 17:1305-1311.
• [3]O'Flaherty JT: Lipid mediators of inflammation and allergy. Lab Invest 1982, 47:314-329.
• [4]Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Canada; 2002.
• [5]Rautava S, Ruuskanen O, Ouwehand A, Salminen S, Isolauri E: The hygiene hypothesis of atopic disease–an extended version. J Pediatr Gastroenterol Nutr 2004, 38:378-388.
• [6]Bjorksten B, Sepp E, Julge K, Voor T, Mikelsaar M: Allergy development and the intestinal microflora during the first year of life. J Allergy Clin Immunol 2001, 108:516-520.
• [7]Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E: Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 2001, 107:129-134.
• [8]Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Müller G, Stokholm J, Smith B, Krogfelt KA: Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol 2011, 128:646-652.
• [9]Abrahamsson TR, Jakobsson HE, Andersson AF, Björkstén B, Engstrand L, Jenmalm MC: Low diversity of the gut microbiota in infants with atopic eczema. J Allergy Clin Immunol 2012, 129:434-440.
• [10]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, 357:1076-1079.
• [11]Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M: Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 2005, 60:494-500.
• [12]Weston S, Halbert A, Richmond P, Prescott SL: Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child 2005, 90:892-897.
• [13]Taylor AL, Dunstan JA, Prescott SL: Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol 2007, 119:184-191.
• [14]Michail SK, Stolfi A, Johnson T, Onady GM: Efficacy of probiotics in the treatment of pediatric atopic dermatitis: a meta-analysis of randomized controlled trials. Ann Allergy Asthma Immunol 2008, 101:508-516.
• [15]Ismail IH, Licciardi PV, Tang ML: Probiotic effects in allergic disease. J Paediatr Child Health 2013, 49:709-715.
• [16]Helin T, Haahtela S, Haahtela T: No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy 2002, 57:243-246.
• [17]Tamura M, Shikina T, Morihana T, Hayama M, Kajimoto O, Sakamoto A, Kajimoto Y, Watanabe O, Nonaka C, Shida K, Nanno M: Effects of probiotics on allergic rhinitis induced by Japanese cedar pollen: randomized double-blind, placebo-controlled clinical trial. Int Arch Allergy Immunol 2007, 143:75-82.
• [18]Wang MF, Lin HC, Wang YY, Hsu CH: Treatment of perennial allergic rhinitis with lactic acid bacteria. Pediatr Allergy Immunol 2004, 15:152-158.
• [19]Peng GC, Hsu CH: The efficacy and safety of heat-killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house-dust mite. Pediatr Allergy Immunol 2005, 16:433-438.
• [20]Xiao JZ, Kondo S, Yanagisawa N, Takahashi N, Odamaki T, Iwabuchi N, Miyaji K, Iwatsuki K, Togashi H, Enomoto K, Enomoto T: Probiotics in the treatment of Japanese cedar pollinosis: a double-blind placebo-controlled trial. Clin Exp Allergy 2006, 36:1425-1435.
• [21]Ivory K, Chambers SJ, Pin C, Prieto E, Arques JL, Nicoletti C: Oral delivery of Lactobacillus casei Shirota modifies allergen-induced immune responses in allergic rhinitis. Clin Exp Allergy 2008, 38:1282-1289.
• [22]Singh A, Hacini-Rachinel F, Gosoniu ML, Bourdeau T, Holvoet S, Doucet-Ladeveze R, Beaumont M, Mercenier A, Nutten S: Immune-modulatory effect of probiotic Bifidobacterium lactis NCC2818 in individuals suffering from seasonal allergic rhinitis to grass pollen: an exploratory, randomized, placebo-controlled clinical trial. Eur J Clin Nutr 2013, 67:161-167.
• [23]Wassenberg J, Nutten S, Audran R, Barbier N, Aubert V, Moulin J, Mercenier A, Spertini F: Effect of Lactobacillus paracasei ST11 on a nasal provocation test with grass pollen in allergic rhinitis. Clin Exp Allergy 2011, 41:565-573.
• [24]Ouwehand AC, Nermes M, Collado MC, Rautonen N, Salminen S, Isolauri E: Specific probiotics alleviate allergic rhinitis during the birch pollen season. World J Gastroenterol 2009, 15:3261-3268.
• [25]Deruaz C, Leimgruber A, Berney M, Pradervand E, Spertini F: Levocetirizine better protects than desloratadine in a nasal provocation with allergen. J Allergy Clin Immunol 2004, 113:669-676.
• [26]Zweiman B, Getsy J, Kalenian M, Lane A, Schwartz LB, Doty R, Lanza D: Nasal airway changes assessed by acoustic rhinometry and mediator release during immediate and late reactions to allergen challenge. J Allergy Clin Immunol 1997, 100:624-631.
• [27]Ganslmayer M, Spertini F, Rahm F, Terrien MH, Mosimann B, Leimgruber A: Evaluation of acoustic rhinometry in a nasal provocation test with allergen. Allergy 1999, 54:974-979.
• [28]Terrien MH, Rahm F, Fellrath JM, Spertini F: Comparison of the effects of terfenadine with fexofenadine on nasal provocation tests with allergen. J Allergy Clin Immunol 1999, 103:1025-1030.
• [29]Erin EM, Zacharasiewicz AS, Nicholson GC, Tan AJ, Higgins LA, Williams TJ, Murdoch RD, Durham SR, Barnes PJ, Hansel TT: Topical corticosteroid inhibits interleukin-4, -5 and −13 in nasal secretions following allergen challenge. Clin Exp Allergy 2005, 35:1608-1614.
• [30]Bensch GW, Nelson HS, Borish LC: Evaluation of cytokines in nasal secretions after nasal antigen challenge: lack of influence of antihistamines. Ann Allergy Asthma Immunol 2002, 88:457-462.
• [31]Simpson PJ, Fitzgerald GF, Stanton C, Ross RP: The evaluation of a mupirocin-based selective medium for the enumeration of bifidobacteria from probiotic animal feed. J Microbiol Methods 2004, 57:9-16.
• [32]Ibnou-Zekri N, Schiffrin EJ, Von der Weid T: Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect Immun 2003, 71:428-436.
• [33]Pellaton C, Nutten S, Thierry AC, Boudousquié C, Barbier N, Blanchard C, Corthésy B, Mercenier A, Spertini F: Intragastric and intranasal administration of lactobacillus paracasei NCC2461 modulates allergic airway inflammation in mice. Int J Inflam 2012, 2012:686739.
• [34]Aalberse RC, Stapel SO, Schuurman J, Rispens T: Immunoglobulin G4: an odd antibody. Clin Exp Allergy 2009, 39:469-477.
• [35]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, 38:611-618.
• [36]Vliagoftis H, Kouranos VD, Betsi GI, Falagas ME: Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trials. Ann Allergy Asthma Immunol 2008, 101:570-579.
• [37]Miettinen M, Veckman V, Latvala S, Sareneva T, Matikainen S, Julkunen I: Live Lactobacillus rhamnosus and Streptococcus pyogenes differentially regulate Toll-like receptor (TLR) gene expression in human primary macrophages. J Leukoc Biol 2008, 84:1092-1100.
• [38]Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, Julkunen I: Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun 1998, 66:6058-6062.
• [39]Amati L, Pepe M, Passeri ME, Mastronardi ML, Jirillo E, Covelli V: Toll-like receptor signaling mechanisms involved in dendritic cell activation: potential therapeutic control of T cell polarization. Curr Pharm Des 2006, 12:4247-4254.
• [40]Ozdemir C, Akdis M, Akdis CA: T-cell response to allergens. Chem Immunol Allergy 2010, 95:22-44.
• [41]Schmidt-Weber CB, Akdis M, Akdis CA: TH17 cells in the big picture of immunology. J Allergy Clin Immunol 2007, 120:247-254.