Journal of Otolaryngology and Ophthalmology of Shandong University ›› 2021, Vol. 35 ›› Issue (3): 70-80.doi: 10.6040/j.issn.1673-3770.0.2020.374

Previous Articles     Next Articles

Therapeutic and anti-allergic effects of probiotics on allergic rhinitis: a meta-analysis

LIN Xiaoyan, LI Jing, MA Zhiqi, LI Yilin, GAO Xinyi, LI Yong   

  1. Affiliated Hangzhou First People's Hospital, Zhejiang University School of Medicine, Hangzhou 310000, Zhejiang, China
  • Published:2021-05-14

Abstract: Objective To systemically review the therapeutic and anti-allergic effects of probiotics on allergic rhinitis(AR). Methods Publications from PubMed, the Cochrane Library, Embase, CNKI, WanFang, and VIP databases were searched from inception to February 2020. Two reviewers extracted the data and performed literature evaluation. Revman 5.3 software was used for meta-analysis. Results A total of 27 randomized controlled trials comprising 2 147 patients(1 106 patients in the probiotics group and 1 041 patients in the placebo group)were included. The results of meta-analysis showed that probiotics reduced serum total IgE [SMD=-0.22, 95%CI(-0.42, -0.02), P=0.03<0.05] and eosinophil level [SMD=-0.38, 95%CI(-0.69, -0.08), P=0.01<0.05]. Rhinoconjunctivitis quality of life questionnaire(RQLQ)nose symptoms [MD=-0.78, 95%CI(-0.96, -0.61), P<0.001], RQLQ eye symptoms [MD=-0.78, 95%CI(-0.96, -0.61), P<0.000 01], the total nasal symptom score [MD=-1.54, 95%CI(-1.77, -1.31), P<0.001], and medication scores [SMD=-0.43, 95%CI(-0.64, -0.22), P<0.001] were significantly lower in the placebo group. However, specific IgE [SMD=0.08, 95%CI(-0.11, 0.26), P=0.42] and Th1/Th2 ratio [SMD=0.40,95%CI(-1.20, 1.99), P=0.63] were not statistically different between the groups. Conclusion Probiotics effectively reduced symptom scores of patients with AR compared with placebo. Although short-term use of probiotics showed no significant preventive effects on AR, their long-term use reduced serum total IgE level and eosinophil count. Taken together, probiotics can be suggested as an effective treatment for AR.

Key words: Probiotics, Allergic rhinitis, Randomized controlled trials, Efficacy, IgE, Th1/Th2, Eosinophil, Meta-analysis

CLC Number: 

  • R765
[1] Seidman MD, Gurgel RK, Lin SY, et al. Clinical practice guideline: Allergic rhinitis[J]. Otolaryngol Head Neck Surg, 2015, 152(1 suppl): S1-43. doi:10.1177/0194599814561600.
[2] Bousquet J, Schünemann HJ, Togias A, 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[J]. J Allergy Clin Immunol, 2020, 145(1): 70-80.e3. doi:10.1016/j.jaci.2019.06.049.
[3] Wallace DV, Dykewicz MS, Oppenheimer J, et al. Pharmacologic treatment of seasonal allergic rhinitis: synopsis of guidance from the 2017 joint task force on practice parameters[J]. Ann Intern Med, 2017, 167(12): 876. doi:10.7326/m17-2203.
[4] Yan F, Polk DB. Probiotics and immune health[J]. Curr Opin Gastroenterol, 2011, 27(6): 496-501. doi:10.1097/mog.0b013e32834baa4d.
[5] Colbey C, Cox AJ, Pyne DB, et al. Upper respiratory symptoms, gut health and mucosal immunity in Athletes[J]. Sports Med, 2018, 48(1): 65-77. doi:10.1007/s40279-017-0846-4.
[6] Dennis-Wall JC, Culpepper T, Nieves C, 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[J]. Am J Clin Nutr, 2017, 105(3): 758-767. doi:10.3945/ajcn.116.140012.
[7] Chen YS, Jan RL, Lin YL, et al. Randomized placebo-controlled trial of Lactobacillus on asthmatic children with allergic rhinitis[J]. Pediatr Pulmonol, 2010, 45(11): 1111-1120. doi:10.1002/ppul.21296.
[8] Ciprandi G, Vizzaccaro A, Cirillo I, et al. Bacillus clausii effects in children with allergic rhinitis[J]. Allergy, 2005, 60(5): 702-703. doi:10.1111/j.1398-9995.2005.00722.x.
[9] Miraglia del Giudice M, Indolfi C, Capasso M, 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[J]. Italian J Pediatr, 2017, 43(1): 1-6. doi:10.1186/s13052-017-0340-5.
[10] Costa DJ, Marteau P, Amouyal 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)[J]. Eur J Clin Nutr, 2014, 68(5): 602-607. doi:10.1038/ejcn.2014.13.
[11] Giovannini M, Agostoni C, Riva E, 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[J]. Pediatr Res, 2007, 62(2): 215-220. doi:10.1203/pdr.0b013e3180a76d94.
[12] Ishida Y, Nakamura F, Kanzato H, et al. Effect of milk fermented with Lactobacillus acidophilus strain L-92 on symptoms of Japanese cedar pollen allergy: a randomized placebo-controlled trial[J]. Biosci Biotechnol Biochem, 2005, 69(9): 1652-1660. doi:10.1271/bbb.69.1652.
[13] Ishida Y, Nakamura F, Kanzato H, et al. Clinical effects of Lactobacillus acidophilus strain L-92 on perennial allergic rhinitis: a double-blind, placebo-controlled study[J]. J Dairy Sci, 2005, 88(2): 527-533. doi:10.3168/jds.S0022-0302(05)72714-4.
[14] Lin WY, Fu LS, Lin HK, 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[J]. Pediatr Neonatol, 2014, 55(3): 181-188. doi:10.1016/j.pedneo.2013.10.001.
[15] Lin TY, Chen CJ, Chen LK, et al. Effect of probiotics on allergic rhinitis in Df, Dp or dust-sensitive children: a randomized double blind controlled trial[J]. Indian Pediatr, 2013, 50(2): 209-213. doi:10.1007/s13312-013-0068-2.
[16] Kawase M, He F, Kubota A, et al. Effect of fermented milk prepared with two probiotic strains on Japanese cedar pollinosis in a double-blind placebo-controlled clinical study[J]. Int J Food Microbiol, 2009, 128(3): 429-434. doi:10.1016/j.ijfoodmicro.2008.09.017.
[17] Meng Q, Li P, Li Y, et al. Broncho-vaxom alleviates persistent allergic rhinitis in patients by improving Th1/Th2 cytokine balance of nasal mucosa[J]. Rhinology, 2019, 57(6): 451-459. doi:10.4193/rhin19.161.
[18] Moreira A, Kekkonen R, Korpela R, et al. Allergy in marathon runners and effect of Lactobacillus GG supplementation on allergic inflammatory markers[J]. Respir Med, 2007, 101(6): 1123-1131. doi:10.1016/j.rmed.2006.11.015.
[19] Nishimura I, Igarashi T, Enomoto T, et al. Clinical efficacy of halophilic lactic acid bacterium Tetragenococcus halophilus Th221 from soy sauce moromi for perennial allergic rhinitis[J]. Allergol Int, 2009, 58(2): 179-185. doi:10.2332/allergolint.O-08-548.
[20] Ogawa T, Hashikawa S, Asai Y, et al. A new synbiotic, Lactobacillus casei subsp.caseitogether with dextran, reduces murine and human allergic reaction[J]. FEMS Immunol Med Microbiol, 2006, 46(3): 400-409. doi:10.1111/j.1574-695x.2006.00046.x.
[21] Peng GC, Hsu CH. The efficacy and safety of heat-killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house-dust mite[J]. Pediatr Allergy Immunol, 2005, 16(5): 433-438. doi:10.1111/j.1399-3038.2005.00284.x.
[22] Tamura M, Shikina T, Morihana T, et al. Effects of probiotics on allergic rhinitis induced by Japanese cedar pollen: randomized double-blind, placebo-controlled clinical trial[J]. Int Arch Allergy Immunol, 2007, 143(1): 75-82. doi:10.1159/000098318.
[23] Wang MF, Lin HC, Wang YY, et al. Treatment of perennial allergic rhinitis with lactic acid bacteria[J]. Pediatr Allergy Immunol, 2004, 15(2): 152-158. doi:10.1111/j.1399-3038.2004.00156.x.
[24] Xiao JZ, Kondo S, Yanagisawa 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]. J Investig Allergol Clin Immunol, 2006, 16(2): 86-93.
[25] Xiao JZ, Kondo S, Yanagisawa N, et al. Probiotics in the treatment of Japanese cedar pollinosis: a double-blind placebo-controlled trial[J]. Clin Exp Allergy, 2006, 36(11): 1425-1435. doi:10.1111/j.1365-2222.2006.02575.x.
[26] Gotoh M, Sashihara T, Ikegami S, et al. Efficacy of oral administration of a heat-killed Lactobacillus gasseri OLL2809 on patients of Japanese cedar pollinosis with high Japanese-cedar pollen-specific IgE[J]. Biosci Biotechnol Biochem, 2009, 73(9): 1971-1977. doi:10.1271/bbb.90144.
[27] Yonekura S, Okamoto Y, Okawa T, et al. Effects of daily intake of Lactobacillus paracasei strain KW3110 on Japanese cedar pollinosis[J]. Allergy Asthma Proc, 2009, 30(4): 397-405. doi:10.2500/aap.2009.30.3256.
[28] Nagata Y, Yoshida M, Kitazawa H, et al. Improvements in seasonal allergic disease with Lactobacillus plantarum no. 14[J]. Biosci Biotechnol Biochem, 2010, 74(9): 1869-1877. doi:10.1271/bbb.100270.
[29] Lue KH, Sun HL, Lu KH, et al. A trial of adding Lactobacillus johnsonii EM1 to levocetirizine for treatment of perennial allergic rhinitis in children aged 7-12 years[J]. Int J Pediatr Otorhinolaryngol, 2012, 76(7): 994-1001. doi:10.1016/j.ijporl.2012.03.018.
[30] Singh A, Hacini-Rachinel F, Gosoniu ML, 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[J]. Eur J Clin Nutr, 2013, 67(2): 161-167. doi:10.1038/ejcn.2012.197.
[31] Dölle S, Berg J, Rasche C, et al. Tolerability and clinical outcome of coseasonal treatment with Escherichia coli Strain nissle 1917 in grass pollen-allergic subjects[J]. Int Arch Allergy Immunol, 2014, 163(1): 29-35. doi:10.1159/000356328.
[32] 陈红江, 高明华, 邹帆, 等. 特异益生菌株对变应性鼻炎患者的免疫调节作用[J]. 第三军医大学学报, 2015, 37(2): 154-157. doi:10.16016/j.1000-5404.201408120. CHEN Hongjiang, GAO Minghua, ZOU Fan, et al. Immunomodulation effect of specific probiotics in allergic rhinitis patients[J]. Journal of Third Military Medical University, 2015, 37(2): 154-157. doi:10.16016/j.1000-5404.201408120.
[33] Kim HJ, Kim HY, Lee SY, et al. Clinical efficacy and mechanism of probiotics in allergic diseases[J]. Korean J Pediatr, 2013, 56(9): 369-376. doi:10.3345/kjp.2013.56.9.369.
[34] Zhou Z, Chen X, Sheng H, et al. Engineering probiotics as living diagnostics and therapeutics for improving human health[J]. Microb Cell Fact, 2020, 19(1): 56. doi:10.1186/s12934-020-01318-z.
[35] 张清照, 嶋田貴志, 程雷,等. 肠球菌属益生菌提取物LFK对变应性鼻炎小鼠血清IL-12的影响[J]. 山东大学耳鼻喉眼学报, 2014, 28(3): 7-9. doi:10.6040/j.issn.1673-3770.0.2014.154. ZHANG Qingzhao, SHIMADA Takashi, CHENG Lei, et al. Effect of lysed enterococcus faecalis FK-23(LFK)on serum IL-12 in allergic rhinitis mice[J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2014, 28(3): 7-9.doi:10.6040/j.issn.1673-3770.0.2014.154.
[36] Vliagoftis H, Kouranos VD, Betsi GI, et al. Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trials[J]. Ann Allergy Asthma Immunol, 2008, 101(6): 570-579. doi:10.1016/S1081-1206(10)60219-0.
[1] YANG Guanying, LI Yuanbin. Advances in the application of artificial intelligence to dry eye disease management [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(3): 115-120.
[2] FANG Lu, LEI Yudan, WANG Hua. Meta-analysis of clinical effect of cyclosporine eye drops in combination with sodium hyaluronate eye drops in the treatment of dry eye syndrome [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(2): 65-73.
[3] LYU Qian, TANG Yuan, GU Zijun, SHI Sailei, LIU Ping, WAN Wenjin. Current status of benefit finding among patients with allergic rhinitis and its influence factors [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 21-28.
[4] LEI Yudan, FANG Lu, CHEN Jian, PENG Changfu. Meta-analysis of clinical Efficacy of tocilizumab in the treatment of moderate-to-severe thyroid-associated ophthalmopathy with steroid resistance or intolerance [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 54-67.
[5] ZHU Mingqiong, LI Zheng, LIU Ru, TIAN Tao, PENG Jingli, LYU Qianyi, TAN Huaxia. The application of AI screening system based on OCT/OCTA in the evaluation of the effect of anti VEGF treatment in patients with diabetes macular edema [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 68-73.
[6] SUN Qingzhu, SHEN Jian, CHEN Xing, WU Yanbing, ZENG Lun. The role of metabolic indicators in predicting ranibizumab efficacy in diabetic macular edema [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 74-81.
[7] GU Min, LU Meiping. Advances in the application of nanomedicine delivery systems in allergen immunotherapy for allergic rhinitis [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 106-111.
[8] CHENG Zhuo, LIANG Hui, XING Lumin. Research progress and prospect analysis of deep learning technology in the application of pharyngeal and laryngeal endoscopy [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2026, 40(1): 112-119.
[9] QIN Nana, LI Yufen, SUN Yuhao, WEI Jian, LI Qin. Effect of interleukin-13 receptor-α2 on nasal mucosal remodeling in rats with allergic rhinitis by TGF-β1/Smad signaling pathway [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(6): 71-77.
[10] DU Kangli, ZHENG Zhenyu, XU Zhanjiang, ZHANG Yu, CHEN Lu, LU Mengyao. Construction and validation of risk prediction model for nasal septal deviation complicated with chronic sinusitis [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(6): 78-86.
[11] XIONG Qin, ZHANG Yan, WU Rina, LI Feng, TANG Lixing. Application of intranasal corticosteroids in pediatrics [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(6): 160-167.
[12] XU Xuemeng, FAN Lei, YU Wangbo, JIANG Zhiyue, PAN Chen, HUANG Yongqin. Meta-analysis of the efficacy of omalizumab in combination with specific immunotherapy for allergic rhinitis [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(5): 26-33.
[13] HUANG Huan, HUA Hongli, DENG Yuqin, JIANG Chengyang, WANG Yuwei, YANG Xinghai. Correlation of allergic rhinitis, tonsil adenoid hypertrophy, and sinusitis in children and analysis of its clinical guiding value [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(5): 34-41.
[14] LIU Yijun, GU Yue, GUAN Dayu, YANG Yucheng, SHEN Yang. The long-term clinical efficacy and safety of vidian neurectomy in refractory allergic rhinitis [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(5): 42-48.
[15] YIN Zhenqian, HUANGFU Hui. Kimura disease:a case report and literature review [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2025, 39(5): 104-107.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!