Journal of Otolaryngology and Ophthalmology of Shandong University ›› 2024, Vol. 38 ›› Issue (6): 78-84.doi: 10.6040/j.issn.1673-3770.0.2024.111

• Clinical Research • Previous Articles    

Study of the association between salivary microbiota and reflux symptoms in patients with laryngopharyngeal reflux

CUI Xiaohuan1-6, YIN Longlong7, ZHANG Yanping1-6, JIANG Xingwang1-6, LI Lina1-6   

  1. 1. Senior Department of Otolaryngology Head and Neck Surgery, the Sixth Medical Center of Chinese PLA General Hospital, Beijing 100037, China2. State Key Laboratory of Hearing and Balance Science, Beijing 100853, China3. National Clinical Research Center for Otolaryngologic Diseases, Beijing 100853, China4. Key Laboratory of Hearing Science, Ministry of Education, Beijing 100853, China5. Beijing Key Laboratory of Hearing Impairment Prevention and Treatment, Beijing 100853, China6. Department of Otolaryngology Head and Neck Surgery, the Eighth Medical Center of Chinese PLA General Hospital, Beijing 100091, China7. Hebei North University, Zhangjiakou 075051, Hebei, China
  • Published:2024-12-13

PDF (PC)

8

Abstract: Objective To investigate the correlation between salivary microbiota and symptoms in laryngopharyngeal reflux(LPR)patients. Methods Patients with a reflux symptom index(RSI)score>13 and an apparent response after 8 weeks of proton pump inhibitor medication were enrolled as the LPR group in the Department of Otorhinolaryngology Head and Neck Surgery, the Eighth Medical Center, Chinese PLA General Hospital from February 2022 to November 2022. Another 34 matched healthy volunteers were enrolled as the control group. Their saliva samples were collected, and salivary microbiota was detected and analysed by 16S rRNA gene sequencing. The correlation between differential bacteria in LEfSe analysis and RSI scores was investigated. SPSS 25.0 software was used for statistical analysis. Results LEfSe difference analysis showed that Lactobacillus_murinus, Lactobacillaceae, Lactobacillus, Prevotellaceae, Prevotella, Bacteroidales, Bacteroidia, Bacteroidetes and other 30 species were enriched in the LPR group. Firmicutes, Bacilli, Pseudomonas and other 28 species were enriched in the control group. The correlation analysis demonstrated that the relative abundance of Bacteroidetes, Bacteroidetes, Bacteroidetes, Prevotellaceae and Prevotella were positively correlated with the symptom score of gastric burning sensation, chest pain, dyspepsia or stomachache, and the relative abundance of Prevotella was significantly correlated with the above symptoms(P<0.05). The relative abundance of Prevotella_oralis was positively correlated with the symptom score of difficulty to swallow food, liquids, and tablets(P<0.05). The relative abundance of Lactobacillaceae and Lactobacillu was negatively related to the total score of RSI. Conclusion The salivary dysbiosis might be related to the reflux symptoms of LPR patients and modify the imbalance of ecology in saliva might help to alleviate the symptoms.

Key words: Laryngopharyngeal reflux, Salivary microbiota, Reflux symptom index, Correlation analysis

CLC Number: 

  • R766.5
[1] Lechien JR, Akst LM, Hamdan AL, et al. Evaluation and management of laryngopharyngeal reflux disease: state of the art review[J]. Otolaryngol Head Neck Surg, 2019, 160(5): 762-782. doi:10.1177/0194599819827488
[2] Xiao SF, Li JR, Zheng HL, et al. An epidemiological survey of laryngopharyngeal reflux disease at the otorhinolaryngology-head and neck surgery clinics in China[J]. Eur Arch Otorhinolaryngol, 2020, 277(10): 2829-2838. doi:10.1007/s00405-020-06045-0
[3] Belstrøm D. The salivary microbiota in health and disease[J]. J Oral Microbiol, 2020, 12(1): 1723975. doi:10.1080/20002297.2020.1723975
[4] Chen T, Yu WH, Izard J, et al. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information[J]. Database, 2010, 2010: baq013. doi:10.1093/database/baq013
[5] Graves DT, Corrêa JD, Silva TA. The oral microbiota is modified by systemic diseases[J]. J Dent Res, 2019, 98(2): 148-156. doi:10.1177/0022034518805739
[6] Li X, Kolltveit KM, Tronstad L, et al. Systemic diseases caused by oral infection[J]. Clin Microbiol Rev, 2000, 13(4): 547-558. doi:10.1128/CMR.13.4.547
[7] Nakano K, Hokamura K, Taniguchi N, et al. The collagen-binding protein of Streptococcus mutans is involved in haemorrhagic stroke[J]. Nat Commun, 2011, 2: 485. doi:10.1038/ncomms1491
[8] 崔小缓, 尹龙龙, 张延平, 等. 咽喉反流患者唾液菌群初步研究[J]. 中华耳鼻咽喉头颈外科杂志, 2023, 58(6): 572-578. doi:10.3760/cma.j.cn115330-20230224-00084 CUI Xiaohuan, YIN Longlong, ZHANG Yanping, et al. A preliminary study on salivary microbiota of patients with laryngopharyngeal reflux[J]. Chinese Journal of Otorhinolaryngology Head and Neck Surgery, 2023, 58(6): 572-578. doi:10.3760/cma.j.cn115330-20230224-00084
[9] Chen H, Wang H, Yang F, et al. Distinct microbiota dysbiosis in patients with. laryngopharynx reflux disease compared to healthy controls[J]. Eur Arch Otorhinolaryngol, 2022, 279(7): 3569-3579. doi: 10.1007/s00405-022-07327-5.
[10] 陈函, 杨帆, 王茂鑫, 等. 咽喉反流性疾病患者症状与体征的关系及相关危险因素研究[J]. 听力学及言语疾病杂志, 2022, 30(6): 573-576. doi:10.3969/j.issn.1006-7299.2022.06.001 CHEN Han, YANG Fan, WANG Maoxin, et al. Study on the relationship between symptoms and signs and related risk factors in patients with laryngopharyngeal reflux disease[J]. Journal of Audiology and Speech Pathology, 2022, 30(6): 573-576. doi:10.3969/j.issn.1006-7299.2022.06.001
[11] 崔小缓, 张延平, 阎小妍, 等. 耳鼻咽喉科门诊成年患者的睡眠状况与咽喉反流性疾病的相关性[J]. 中华耳鼻咽喉头颈外科杂志, 2019, 54(10): 754-759. doi:10.3760/cma.j.issn.1673-0860.2019.10.009 CUI Xiaohuan, ZHANG Yanping, YAN Xiaoyan, et al. Relationship between sleep status and laryngopharyngeal reflux disease in adult patients in Otolaryngology clinic[J]. Chinese Journal of Otorhinolaryngology Head and Neck Surgery, 2019, 54(10): 754-759. doi:10.3760/cma.j.issn.1673-0860.2019.10.009
[12] Haworth JJ, Boyle N, Vales A, et al. The prevalence of intestinal dysbiosis in patients referred for antireflux surgery[J]. Surg Endosc. 2021;35(12):7112-7119. doi:10.1007/s00464-020-08229-5
[13] Zhong L, Shanahan ER, Raj A, et al. Dyspepsia and the microbiome: time to focus on the small intestine[J]. Gut. 2017;66(6):1168-1169. doi:10.1136/gutjnl-2016-312574
[14] Zhu H, Yip H C, Cheung M K, et al. Convergent dysbiosis of upper aerodigestive microbiota between patients with esophageal and oral cavity squamous cell carcinoma[J]. Int J Cancer, 2023. 152(9):1903-1915,doi:/10.1002/ijc.34460.
[15] Copeland E, Leonard K, Carney R, et al. Chronic rhinosinusitis: potential role of microbial dysbiosis and recommendations for sampling sites[J]. Front Cell Infect Microbiol, 2018, 8: 57. doi:10.3389/fcimb.2018.00057
[16] Petersen C, Round JL. Defining dysbiosis and its influence on host immunity and disease[J]. Cell Microbiol, 2014, 16(7): 1024-1033. doi:10.1111/cmi.12308
[17] Zheng XW, Zheng YJ, Chen T, et al. Effect of laryngopharyngeal reflux and potassium-competitive acid blocker(P-CAB)on the microbiological comprise of the laryngopharynx[J]. Otolaryngol Head Neck Surg, 2024, 170(5): 1380-1390. doi:10.1002/ohn.682
[18] Haworth JJ, Boyle N, Vales A, et al. The prevalence of intestinal dysbiosis in patients referred for antireflux surgery[J]. Surg Endosc, 2021, 35(12): 7112-7119. doi:10.1007/s00464-020-08229-5
[19] Lechien JR, De Vos N, Everard A, et al. Laryngopharyngeal reflux: the microbiota theory[J]. Med Hypotheses, 2021, 146: 110460. doi:10.1016/j.mehy.2020.110460
[20] Tett A, Pasolli E, Masetti G, et al. Prevotella diversity, niches and interactions with the human host[J]. Nat Rev Microbiol, 2021, 19(9): 585-599. doi:10.1038/s41579-021-00559-y
[21] Kianoush N, Adler CJ, Nguyen KA, et al. Bacterial profile of dentine caries and the impact of pH on bacterial population diversity[J]. PLoS One, 2014, 9(3): e92940. doi:10.1371/journal.pone.0092940
[22] Liang T, Liu F, Liu LJ, et al. Effects of Helicobacter pylori infection on the oral microbiota of reflux esophagitis patients[J]. Front Cell Infect Microbiol, 2021, 11: 732613. doi:10.3389/fcimb.2021.732613
[23] Sazanskaya LS, Gulua MM, Gilmiyarov EM, et al. The dental status of patients with gastroesophageal reflux disease depending on the intake of proton pump inhibitors[J]. Stomatologiia, 2020, 99(5): 25-31. doi:10.17116/stomat20209905125
[24] Krishnan U, Singh H, Tedla N, et al. Presence of gastric pepsinogen in the Trachea is associated with altered inflammation and microbial composition[J]. Infect Immun, 2020, 88(12): e00455-e00420. doi:10.1128/IAI.00455-20
[25] Park CH, Lee SK. Exploring esophageal microbiomes in esophageal diseases: a systematic review[J]. J Neurogastroenterol Motil, 2020, 26(2): 171-179. doi:10.5056/jnm19240
[26] Kõll P, Mändar R, Marcotte H, et al. Characterization of oral lactobacilli as potential probiotics for oral health[J]. Oral Microbiol Immunol, 2008, 23(2): 139-147. doi:10.1111/j.1399-302X.2007.00402.x
[27] Ahola AJ, Yli-Knuuttila H, Suomalainen T, et al. Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors[J]. Arch Oral Biol, 2002, 47(11): 799-804. doi:10.1016/s0003-9969(02)00112-7
[28] Caglar E, Cildir SK, Ergeneli S, et al. Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets[J]. Acta Odontol Scand, 2006, 64(5): 314-318. doi:10.1080/00016350600801709
[29] Bernard JN, Chinnaiyan V, Almeda J, et al. Lactobacillus sp. facilitate the repair of DNA damage caused by bile-induced reactive oxygen species in experimental models of gastroesophageal reflux disease[J]. Antioxidants, 2023, 12(7): 1314. doi:10.3390/antiox12071314
[30] Aiba, Nakano Y, Koga Y, et al. A highly acid-resistant novel strain of Lactobacillus johnsonii No. 1088 has antibacterial activity, including that against Helicobacter pylori, and inhibits gastrin-mediated acid production in mice[J]. Microbiologyopen, 2015, 4(3): 465-474. doi:10.1002/mbo3.252
[1] WU Wei, WANG Lei, CHEN Sheng, LI Lianyong, WANG Gang. Multidisciplinary research and advances in gastro-oesophageal reflux disease [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 1-14.
[2] LIU Lianlian, LI Jinrang. Obstructive sleep apnea and laryngopharyngeal reflux [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 15-22.
[3] ZHANG Li, ZHANG Mengru, Alimire Aierken, QIU Zhongmin. Role of pharyngeal reflux in common respiratory diseases [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 23-29.
[4] HU Zhiwei, CHEN Dong, YANG Dong, WU Jimin. Diagnosis and treatment of gastroesophageal airway reflux disease: based on related consensus and guidelines from 2020 to 2024 [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 30-38.
[5] ZHAO Jianing, CUI Yuanxin, WANG Dan, ZHAO Ming. Exploration of the relationship between laryngopharyngeal reflux and recurrent respiratory papilloma and its mechanism [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 39-45.
[6] ZHANG Shan, CHEN Qiu, ZHOU Fangwei, MA Yifei. Research progress of biomarkers in laryngopharyngeal reflux disease [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 46-54.
[7] ZHOU Shitong, YANG Yanyan, YANG Yucheng, FANG Hongyan. Pepsin and laryngopharyngeal reflux disease: from pathogenic mechanisms to potential risk factors for pharyngeal and laryngeal squamous cell carcinoma [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 55-60.
[8] XI Xiaoyu, SUI Xinke, CHEN Sheng, LI Lianyong, ZHONG Changqing. Endoscopic treatment of laryngopharyngeal reflux disease [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 61-65.
[9] NIU Yanyan, GU Wei, JIN Xiaofeng, HUO Hong, YANG Dahai, CUI Tingting, WANG Jian. Expression analysis of pepsin in vocal cord leukoplakia tissues [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 66-70.
[10] WANG Lei, WANG Gang, SUN Zhezhe, LIU Hongdan, HAN Haolun, LI Baowei, ZHANG Xiaoli, WU Wei. Correlations between vocal cord hyperplastic lesions, vocal cord leukoplakia, chronic laryngopharyngitis, and laryngopharyngeal reflux [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2024, 38(6): 71-77.
[11] WANG Lei, LI Baowei, WANG Gang, LIU Hongdan, HAN Haolun, ZHANG Xiaoli, WU Wei. A preliminary study on nocturnal alkali reflux in OSAHS patients [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2023, 37(6): 75-79.
[12] ZHOU Xiaoqing, YAN Yajie, LI Yingchun. Treatment of hoarseness based on physiological function of the liver [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2023, 37(5): 74-79.
[13] SHAO Na, ZHANG Qingqing, LIU Xiaohong, XIE Meng, GUO Ruixin, MA Sijing, LIU Haiqin, REN Xiaoyong, LUO Huanan. Effects of Helicobacter pylori infection on salivary pepsin concentration in patients with symptomatic laryngopharyngeal reflux [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2022, 36(6): 89-95.
[14] QIN Ming, SUN Zhanwei, WANG Weiwei, LI Shichao, WU Tianyi, WANG Guangke. Efficacy of alkaline isotonic saline in laryngopharyngeal reflux symptom-positive or finding score-positive patients with chronic rhinosinusitis following endoscopic sinus surgery [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2022, 36(3): 147-153.
[15] ZENG Xianting, WANG Guangke, SUN Zhanwei, WU Tianyi, LI Shichao, WANG Weiwei. Postoperative efficacy of proton pump inhibitor in the treatment of difficult-to-treat rhinosinusitis with laryngopharyngeal reflux [J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2022, 36(3): 189-194.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Website Copyright: Editorial Office of Journal of Otolaryngology and Ophthalmology of Shandong University
Address: No.27 Shanda South Road, Jinan, Shandong, China. Post code: 250100 Tel: +86-0531-88366912 Email: ebhxb@sdu.edu.cn Supported by Beijing Magtech Co.Ltd