Systematic review and meta-analysis of probiotics in the treatment of allergic rhinitis

Main Article Content

Shuiping Yan
Si Ai
Lizhen Huang
Caixia Qiu
Fangting Zhang
Ningxin He
Xiangli Zhuang
Jian Zheng

Keywords

allergic rhinitis, meta-analysis, probiotics

Abstract

Background: The purpose of this meta-analysis is to systematically evaluate the efficacy of probiotics on allergic rhinitis (AR).


Methods: Collecting randomized controlled trials (RCTs) with probiotics as intervention measures for AR, two researchers independently screened the literature, extracted the data and evaluated the methodological quality of the included studies, and used RevMan 5.3 software for meta-analysis to observe the effects of probiotics on Rhinitis Quality of Life (RQLQ) scores, Rhinitis Total Symptom Scores (RTSS), blood eosinophil count, total and antigen-specific serum immunoglobulin E (IgE) levels by using the fixed- or the random-effects model to calculate the pooled risk for significant heterogeneity.


Results: A total of 2708 patients were included in 30 RCTs. Meta-analysis results showed that the RQLQ global scores (mean difference [MD] = −9.43; P < 0.00001), RQLQ nasal scores (MD = −1.52; P = 0.03), and RTSS nasal scores (MD = −1.96; P = 0.02) significantly improved in the probiotic group when compared with those in the placebo group. There was no significant difference in blood eosinophil count (MD = −0.09; P=0.82), RQLQ eye scores (MD = −1.45; P = 0.07), RTSS global scores (MD = −2.24; P = 0.26), RTSS eye scores (MD = −0.39; P = 0.31), total and antigen-specific serum IgE levels (MD = −0.04; P = 0.7 and MD = −0.08; P = 0.81) between the probiotic and the placebo group.


Conclusion: Compared with the placebo group, the quality of life and symptoms of patients with AR significantly improved in the probiotic group, thus providing a new potential method for the application of probiotics in AR. However, because of the limited evidence for the current study outcomes, the heterogeneity of research, and the differences in research results, more high-quality studies are needed to in the future.

Abstract 1602 | PDF Downloads 1414 HTML Downloads 109 XML Downloads 27

References

1. Linton S, Burrows AG, Hossenbaccus L, Ellis AK. Future of allergic rhinitis management. Ann Allergy Asthma Immunol. 2021; 127: 183–190. 10.1016/j.anai.2021.04.029

2. Wang XD, Zheng M, Lou HF, Wang CS, Zhang Y, Bo MY, et al. An increased prevalence of self-reported allergic rhinitis in major Chinese cities from 2005 to 2011. Allergy. 2016; 71: 1170–1180. 10.1111/all.12874

3. Kim MJ, Ku S, Kim SY, Lee HH, Jin H, Kang S, et al. Safety evaluations of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI. Int J Mol Sci. 2018; 19:1422. 10.3390/ijms19051422

4. Schaefer M, Enck P. Effects of a probiotic treatment (Enterococcus faecalis) and open-label placebo on symptoms of allergic rhinitis: Study protocol for a randomised controlled trial. BMJ Open. 2019; 9:e031339. 10.1136/bmjopen-2019-031339

5. Zhang J, Shi ZL, Zeng MH, Wei C, Wu HX, Liu MY, et al. Oral administration of Clostridium butyricum CGMCC0313-1 reduces ovalbumin-induced allergic airway inflammation in mice. Respirology. 2017; 22: 898–904. 10.1111/resp.12985

6. Borchers AT, Selmi C, Meyers FJ, Keen CL, Gershwin ME. Probiotics and immunity. J Gastroenterol. 2009;44:26–46. 10.1007/s00535-008-2296-0

7. Ozdemir O. Various effects of different probiotic strains in allergic disorders: An update from laboratory and clinical data. Clin Exp Immunol. 2010;160:295–304. 10.1111/j.1365-2249.2010.04109.x

8. Watts AM, West NP, Smith PK, Cripps AW, Cox AJ. Probiotics and allergic rhinitis: A Simon two-stage design to determine effectiveness. J Altern Complement Med. 2016; 22: 1007–1112. 10.1089/acm.2016.0115

9. Zajac AE, Adams AS, Turner JH. In a systematic review and meta-analysis of probiotics for the treatment of allergic rhinitis. Int Forum Allergy Rhinol. 2015;5:524–532. 10.1002/alr.21492

10. Szajewska H, Horvath A. Lactobacillus rhamnosus GG in the primary prevention of eczema in children: A systematic review and meta-analysis. Nutrients. 2018;10:1319. 10.3390/nu10091319

11. Plummer EL, Chebar LA, Tobin JM, Uebergang JB, Axelrad C, Garland SM, et al. Postnatal probiotics and allergic disease in very preterm infants: Sub-study to the ProPrems randomized trial. Allergy. 2020; 75:127–136. 10.1111/all.14088

12. Zajac AE, Adams AS, Turner JH. A systematic review and meta-analysis of probiotics for the treatment of allergic rhinitis. Int Forum Allergy Rhinol. 2015;5:524–532. 10.1002/alr.21492

13. Clark HD, Wells GA, Huet C, McAlister FA, Salmi LR, Fergusson D. Assessing the quality of randomized trials: Reliability of the Jadad scale. Control Clin Trials. 1999;20: 448–452. 10.1016/S0197-2456(99)00026-4

14. Juniper EF, Thompson AK, Ferrie PJ, Roberts JN. Validation of the standardized version of the rhinoconjunctivitis quality of life questionnaire. J Allergy Clin Immunol. 1999;104:364–369. 10.1016/S0091-6749(99)70380-5

15. Lilly DM and Stillwell RH. Science 1965 Feb 12;147(3659):747-8. 10.1126/science.147.3659.747

16. Yamanishi S, Pawankar R. Current advances on the microbiome and role of probiotics in upper airways disease. Curr Opin Allergy Clin Immunol. 2020;20:30–35. 10.1097/ACI.0000000000000604

17. Watts AM, Cox AJ, Smith PK, Besseling-van der Vaart I, Cripps AW, West NP. A specifically designed multispecies probiotic supplement relieves seasonal allergic rhinitis symptoms. J Altern Complement Med. 2018;24:833–840. 10.1089/acm.2017.0342

18. Kim WG, Kang GD, Kim HI, Han MJ, Kim DH. Bifidobacterium longum IM55 and Lactobacillus plantarum IM76 alleviate allergic rhinitis in mice by restoring Th2/Treg imbalance and gut microbiota disturbance. Benef Microbes. 2019;10:55–67. 10.3920/BM2017.0146

19. Choi SP, Oh HN, Choi CY, Ahn H, Yun HS, Chung YM, et al. Oral administration of Lactobacillus plantarum CJLP133 and CJLP243 alleviates birch pollen-induced allergic rhinitis in mice. J Appl Microbiol. 2018;124:821–828. 10.1111/jam.13635

20. Johansson MA, Bjorkander S, Mata Forsberg M, Qazi KR, Salvany Celades M, Bittmann J, et al. Probiotic lactobacilli modulate Staphylococcus aureus-induced activation of conventional and unconventional T cells and NK Cells. Front Immunol. 2016;7:273. 10.3389/fimmu.2016.00273

21. Enaud R, Prevel R, Ciarlo E, Beaufils F, Wieërs G, Guery B, et al. The gut-lung axis in health and respiratory diseases: A place for inter-organ and inter-kingdom crosstalks. Front Cell Infect Microbiol. 2020;10:9. 10.3389/fcimb.2020.00009

22. Tamura M, Shikina T, Morihana T, Hayama M, Kajimoto O, Sakamoto A, et al. 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.

23. Kang MG, Han SW, Kang HR, Hong SJ, Kim DH, Choi JH. Probiotic NVP-1703 alleviates allergic rhinitis by inducing il-10 expression: A four-week clinical trial. Nutrients. 2020;12:1427. 10.3390/nu12051427

24. Meng Q, Li P, Li Y, Chen J, Wang L, He L, et al. Broncho-vaxom alleviates persistent allergic rhinitis in patients by improving Th1/Th2 cytokine balance of nasal mucosa. Rhinology. 2019;57:451–459. 10.4193/Rhin19.161

25. Miraglia Del Giudice M, Indolfi C, Capasso M, Maiello N, Decimo F, Ciprandi G. Bifidobacterium mixture (B longum BB536, B infantis M-63, B breve M-16V) treatment in children with seasonal allergic rhinitis and intermittent asthma. Ital J Pediatr. 2017;43:1–6. 10.1186/s13052-017-0340-5

26. Dennis-Wall JC, Culpepper T, Nieves C, Rowe CC, Burns AM, Rusch CT, et al. Probiotics (Lactobacillus gasseri KS-13, Bifidobacterium bifidum G9-1, and Bifidobacterium longum MM-2) improve rhinoconjunctivitis-specific quality of life in individuals with seasonal allergies: A double-blind, placebo-controlled, randomized trial. Am J Clin Nutr. 2017;105:758–767. 10.3945/ajcn.116.140012

27. Jerzynska J, Stelmach W, Balcerak J, Woicka-Kolejwa K, Rychlik B, Blauz A, et al. Effect of Lactobacillus rhamnosus GG and vitamin D supplementation on the immunologic effectiveness of grass-specific sublingual immunotherapy in children with allergy. Allergy Asthma Proc. 2016;37:324–334. 10.2500/aap.2016.37.3958

28. Costa DJ, Marteau P, Amouyal M, Poulsen LK, Hamelmann E, Cazaubiel M, et al. Efficacy and safety of the probiotic Lactobacillus paracasei LP-33 in allergic rhinitis: A double-blind, randomized, placebo-controlled trial (GA2LEN Study). Eur J Clin Nutr. 2014; 68:602–607. 10.1038/ejcn.2014.13

29. Lin WY, Fu LS, Lin HK, Shen CY, Chen YJ. 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. Pediatr Neonatol. 2014; 55:181–188. 10.1016/j.pedneo.2013.10.001

30. Singh A, Hacini-Rachinel F, Gosoniu ML, Bourdeau T, Holvoet S, Doucet-Ladeveze R, et al. 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. 10.1038/ejcn.2012.197

31. Lin TY, Chen CJ, Chen LK, Wen SH, Jan RH. Effect of probiotics on allergic rhinitis in Df, Dp or dust-sensitive children: A randomized double blind controlled trial. Indian Pediatr. 2013;50:209–213. 10.1007/s13312-013-0068-2

32. Lue KH, Sun HL, Lu KH, Ku MS, Sheu JN, Chan CH, et al. A trial of adding Lactobacillus johnsonii EM1 to levocetirizine for treatment of perennial allergic rhinitis in children aged 7-12 years. Int J Pediatr Otorhinolaryngol. 2012;76:994–1001. 10.1016/j.ijporl.2012.03.018

33. Chen YS, Jan RL, Lin YL, Chen HH, Wang JY. Randomized placebo-controlled trial of lactobacillus on asthmatic children with allergic rhinitis. Pediatr Pulmonol. 2010;45:1111–1120. 10.1002/ppul.21296

34. 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. 10.3748/wjg.15.3261

35. Nishimura I, Igarashi T, Enomoto T, Dake Y, Okuno Y, Obata A. Clinical efficacy of halophilic lactic acid bacterium Tetragenococcus halophilus Th221 from soy sauce moromi for perennial allergic rhinitis. Allergol Int. 2009;58:179–185. 10.2332/allergolint.O-08-548

36. Giovannini M, Agostoni C, Riva E, Salvini F, Ruscitto A, Zuccotti GV, 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. Pediatr Res. 2007;62:215–220. 10.1203/PDR.0b013e3180a76d94

37. 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. 10.1111/j.1399-3038.2005.00284.x

38. Ciprandi G, Vizzaccaro A, Cirillo I, Tosca MA. Bacillus clausii effects in children with allergic rhinitis. Allergy. 2005;60:702–703. 10.1111/j.1398-9995.2005.00722.x

39. Wang MF, Lin HC, Wang YY, Hsu CH. Treatment of perennial allergic rhinitis with lactic acid bacteria. Pediatr Allergy Immunol. 2004;15:152–158. 10.1111/j.1399-3038.2004.00156.x

40. Harata G, Kumar H, He F, Miyazawa K, Yoda K, Kawase M, et al. Probiotics modulate gut microbiota and health status in Japanese cedar pollinosis patients during the pollen season. Eur J Nutr. 2017; 56: 2245–2253. 10.1007/s00394-016-1264-3

41. Kawase M, He F, Kubota A, Hiramatsu M, Saito H, Ishii T, et al. Effect of fermented milk prepared with two probiotic strains on Japanese cedar pollinosis in a double-blind placebo-controlled clinical study. Int J Food Microbiol. 2009;128:429–434. 10.1016/j.ijfoodmicro.2008.09.017

42. Xiao JZ, Kondo S, Yanagisawa N, Takahashi N, Odamaki T, Iwabuchi N, et al. Effect of probiotic Bifidobacterium longum BB536 [corrected] in relieving clinical symptoms and modulating plasma cytokine levels of Japanese cedar pollinosis during the pollen season. A randomized double-blind, placebo-controlled trial. J Investig Allergol Clin Immunol. 2006; 16:86–93. Available from: https://pubmed.ncbi.nlm.nih.gov/16689181/

43. Xiao JZ, Kondo S, Yanagisawa N, Takahashi N, Odamaki T, Iwabuchi N, et al. Probiotics in the treatment of Japanese cedar pollinosis: A double-blind placebo controlled trial. Clin Exp Allergy. 2006;36:1425–1435. 10.1111/j.1365-2222.2006.02575.x

44. Sadeghi-Shabestari M, Moghaddam YJ, Rezapoor H, Sohrabpour M. Effect of probiotics on allergic rhinitis: A randomized, controlled, clinical trial. Galen Med J. 2020;9: e1918. 10.31661/gmj.v9i0.1918

45. Ahmed M, Billoo AG, Iqbal K. Efficacy of probiotic in perennial allergic rhinitis under five year children: A randomized controlled trial. Pak J Med Sci. 2019; 35(6): 1538–1543. 10.12669/pjms.35.6.744

46. Perrin Y, Nutten S, Audran R, Berger B, Bibiloni R, Wassenberg J, 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. Clin Transl Allergy. 2014;4:1. 10.1186/2045-7022-4-1

47. Xu LZ, Yang LT, Qiu SQ, Yang G, Luo XQ, Miao BP, et al. Combination of specific allergen and probiotics induces specific regulatory B cells and enhances specific immunotherapy effect on allergic rhinitis. Oncotarget. 2016;7:54360–54369. 10.18632/oncotarget.10946

48. Nembrini C, Singh A, De Castro CA, Mercenier A, Nutten S. Oral administration of Lactobacillus paracasei NCC 2461 for the modulation of grass pollen allergic rhinitis: a randomized, placebocontrolled study during the pollen season. Clin Transl Allergy. 2015; 5: 41. 10.1186/s13601-015-0085-4

49. Jan RH, Chen CJ, Chen LK, Wen SH, Lin TY. Is the effect of probiotics on allergic rhinitis confined to Dermatophagoides farinae, Dermatophagoides pteronyssinus, or dust-sensitive children? A randomized prospective double-blind controlled trial. Tzu Chi Medical Journal. 2011; 23: 51–54. 10.1016/j.tcmj.2011.05.003

50. Anania C, Patrizia Di Marino V, Olivero F, De Canditiis D, Brindisi G, Iannilli F, et al. Treatment with a probiotic mixture containing Bifidobacterium animalis Subsp. Lactis BB12 and Enterococcus faecium L3 for the prevention of allergic rhinitis symptoms in children: A randomized controlled trial. Nutrients. 2021;13:1315. 10.3390/nu13041315

51. 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 doubleblind study. Allergy. 2002;57:243–246. 10.1034/j.1398-9995.2002.1s3299.x