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The Profiles of Laryngopharyngeal Reflux in Patients With Different Vocal Fold Lesions

  • Jinhong Zhang
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048

    Department of otolaryngology, School of Medicine, South China University of Technology, Guangzhou, 510006
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  • Xiaoyu Wang
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048
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  • Jiasen Wang
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048
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  • Jing Zhao
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048
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  • Chun Zhang
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048
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  • Zhi Liu
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048
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  • Jinrang Li
    Correspondence
    Address correspondence and reprint requests to Dr. Jinrang Li, Department of Otolaryngology, The Sixth Medical Center of PLA General Hospital, Beijing 100048, China, Phone: 18600310277.
    Affiliations
    Department of otolaryngology, The Sixth Medical Center of PLA General Hospital of Beijing, Beijing, 100048

    Department of otolaryngology, School of Medicine, South China University of Technology, Guangzhou, 510006
    Search for articles by this author
Published:September 01, 2022DOI:https://doi.org/10.1016/j.jvoice.2022.08.002

      Summary

      Objectives

      To investigate the profiles of laryngopharyngeal reflux (LPR) and the relationship between hypopharyngeal-proximal reflux episodes (HREs) and the positive rate of salivary pepsin testing in patients with vocal fold lesions (VFLs).

      Methods

      The enrolled patients were divided into vocal fold cancer group (VFCG), vocal fold leukoplakia group (VFLG), benign vocal fold lesion group (BVFLG) and control group (CG). Patients benefited from multichannel intraluminal impedance-pH monitoring (MII-pH) and multi-time point salivary pepsin testing (MTPSPT). The LPR profiles of patients with VFLs were studied by analyzing the MII-pH findings. The relationship between HREs and positive rate of MTPSPT was investigated through the nonparametric test.

      Results

      177 patients were included. According to 24 h MII-pH, the occurrence of HREs tended to increase after meals. 55.75%, 63.98%, 66.82% and 55.77% of the HREs in the VFCG, VFLG, BVFLG and CG occurred within 3 h after meals, respectively. The overall positive rate of MTPSPT was higher in the VFCG than the remaining groups. In the VFCG, there was a significant correlation between overall positive results of MTPSPT and HREs occurring within 3 h after meals.

      Conclusion

      In the Chinese population, the occurrence of HREs tend to more frequently after meals in patients with VFLs, and most HREs occur within 3 h after meals. By analyzing the 24h MII-pH findings, we can develop a more individualized anti-reflux therapeutic strategy for LPR patients.

      Key Words

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      References

        • Lechien J R
        • Akst L M
        • Hamdan A L
        • et al.
        Evaluation and management of laryngopharyngeal reflux disease: state of the art review.
        Otolaryngol Head Neck Surg. 2019; 160: 762-782https://doi.org/10.1177/0194599819827488
        • Gasiorowska A.
        Protection and regeneration of esophageal, pharyngeal, and laryngeal mucosa as a major element in therapy of patients with esophageal and extraesophageal reflux symptoms.
        Otolaryngol Pol. 2020; 74: 40-45https://doi.org/10.5604/01.3001.0014.3614
        • Zhang M
        • Chia C
        • Stanley C
        • et al.
        Diagnostic utility of salivary pepsin as compared with 24-hour dual pH/impedance probe in laryngopharyngeal reflux.
        Otolaryngol Head Neck Surg. 2021; 164: 375-380https://doi.org/10.1177/0194599820951183
        • Cumpston E C
        • Blumin J H
        • Bock J M
        Dual pH with multichannel intraluminal impedance testing in the evaluation of subjective laryngopharyngeal reflux symptoms.
        Otolaryngol Head Neck Surg. 2016; 155: 1014-1020https://doi.org/10.1177/0194599816665819
        • Wang J
        • Li J
        • Nie Q
        • et al.
        Are multiple tests necessary for salivary pepsin detection in the diagnosis of laryngopharyngeal reflux?.
        Otolaryngol Head Neck Surg. 2021; (1945998211026837)https://doi.org/10.1177/01945998211026837
        • Lu G
        • Ding X
        • Xu W.
        Association between laryngopharyngeal reflux and vocal fold leukoplakia.
        ORL J Otorhinolaryngol Relat Spec. 2021; 83: 159-166https://doi.org/10.1159/000512527
        • Han H
        • Lyu Q
        • Zhao J.
        Laryngopharyngeal reflux in hypertrophic laryngeal diseases.
        Ear Nose Throat J. 2020; 145561320953232https://doi.org/10.1177/0145561320953232
        • Lechien J R
        • Saussez S
        • Harmegnies B
        • et al.
        Laryngopharyngeal Reflux as Causative Factor of Vocal Fold Nodules.
        J Voice. 2020; 34: 150-151https://doi.org/10.1016/j.jvoice.2018.06.006
        • Tan J J
        • Wang L
        • Mo T T
        • et al.
        Pepsin promotes IL-8 signaling-induced epithelial-mesenchymal transition in laryngeal carcinoma.
        Cancer Cell Int. 2019; 19https://doi.org/10.1186/s12935-019-0772-7
        • Niu K
        • Guo C
        • Teng S
        • et al.
        Pepsin promotes laryngopharyngeal neoplasia by modulating signaling pathways to induce cell proliferation.
        PLoS One. 2020; 15e0227408https://doi.org/10.1371/journal.pone.0227408
        • Yin C Y
        • Zhang S S
        • Zhong J T
        • et al.
        Pepsin and laryngeal and hypopharyngeal carcinomas.
        Clin Exp Otorhinolaryngol. 2020; https://doi.org/10.21053/ceo.2020.00465
        • Samuels T L
        • Zimmermann M T
        • Zeighami A
        • et al.
        RNA sequencing reveals cancer-associated changes in laryngeal cells exposed to non-acid pepsin.
        Laryngoscope. 2021; 131: 121-129https://doi.org/10.1002/lary.28636
        • Lewin J S
        • Gillenwater A M
        • Garrett J D
        • et al.
        Characterization of laryngopharyngeal reflux in patients with premalignant or early carcinomas of the larynx.
        Cancer. 2003; 97: 1010-1014https://doi.org/10.1002/cncr.11158
        • Belafsky P C
        • Postma G N
        • Koufman JA
        Validity and reliability of the Reflux Symptom Index (RSI).
        Journal of Voice. 2002; 16: 274-277https://doi.org/10.1016/s0892-1997(02)00097-8
        • Belafsky P C
        • Postma G N
        • Koufman JA.
        The validity and reliability of the reflux finding score (RFS).
        Laryngoscope. 2001; 111: 1313-1317https://doi.org/10.1097/00005537-200108000-00001
        • Hoppo T
        • Sanz A F
        • Nason K S
        • et al.
        How much pharyngeal exposure is "normal"? Normative data for laryngopharyngeal reflux events using hypopharyngeal multichannel intraluminal impedance (HMII).
        J Gastrointest Surg. 2012; 16 (discussion 24-15): 16-24https://doi.org/10.1007/s11605-011-1741-1
        • Johnson L F
        • DeMeester TR.
        Development of the 24-hour intraesophageal pH monitoring composite scoring system.
        J Clin Gastroenterol. 1986; 8: 52-58https://doi.org/10.1097/00004836-198606001-00008
        • Zhang J
        • Li J
        • Zhang Y
        • et al.
        Multitime point pepsin testing can double the rate of the diagnosis of laryngopharyngeal reflux.
        Laryngoscope Investig Otolaryngol. 2021; 6: 1389-1394https://doi.org/10.1002/lio2.700
        • Eells A C
        • Mackintosh C
        • Marks L
        • et al.
        Gastroesophageal reflux disease and head and neck cancers: A systematic review and meta-analysis.
        Am J Otolaryngol. 2020; 41102653https://doi.org/10.1016/j.amjoto.2020.102653
        • Riley C A
        • Marino M J
        • Hsieh M C
        • et al.
        Detection of laryngeal carcinoma in the U.S. elderly population with gastroesophageal reflux disease.
        Head & neck. 2019; 41: 1434-1440https://doi.org/10.1002/hed.25600
        • Wang G
        • Qu C
        • Wang L
        • et al.
        Utility of 24-hour pharyngeal pH monitoring and clinical feature in laryngopharyngeal reflux disease.
        Acta Otolaryngol. 2019; 139: 299-303https://doi.org/10.1080/00016489.2019.1571280
        • El-Serag H B
        • Satia JA
        • Rabeneck L.
        Dietary intake and the risk of gastro-oesophageal reflux disease: a cross sectional study in volunteers.
        Gut. 2005; 54: 11-17https://doi.org/10.1136/gut.2004.040337
        • Lechien J R
        • Bobin F
        • Muls V
        • et al.
        Patients with acid, high-fat and low-protein diet have higher laryngopharyngeal reflux episodes at the impedance-pH monitoring.
        Eur Arch Otorhinolaryngol. 2020; 277: 511-520https://doi.org/10.1007/s00405-019-05711-2
        • Benjamin T
        • Zackria S
        • Lopez R
        • et al.
        Upper esophageal sphincter abnormalities and high-resolution esophageal manometry findings in patients with laryngopharyngeal reflux.
        Scand J Gastroenterol. 2017; 52: 816-821https://doi.org/10.1080/00365521.2017.1322139
        • Lechien J R
        • Crevier-Buchman L
        • Distinguin L
        • et al.
        Is diet sufficient as laryngopharyngeal reflux treatment? A cross-over observational study.
        Laryngoscope. 2021; https://doi.org/10.1002/lary.29890
      1. Kaltenbach T, Crockett S, Gerson L B. Are lifestyle measures effective in patients with gastroesophageal reflux disease? An evidence-based approach. Archives of internal medicine. 2006; 166:965-971. https://doi.org/10.1001/archinte.166.9.965.

        • Bujanda L.
        The effects of alcohol consumption upon the gastrointestinal tract.
        Am J Gastroenterol. 2000; 95: 3374-3382https://doi.org/10.1111/j.1572-0241.2000.03347.x
        • Chattopadhyay D K
        • Greaney M G
        • Irvin T T
        Effect of cigarette smoking on the lower oesophageal sphincter.
        Gut. 1977; 18: 833-835https://doi.org/10.1136/gut.18.10.833
        • Fuchs K H
        • Meining A.
        Current insights in the pathophysiology of gastroesophageal reflux disease.
        Chirurgia (Bucur). 2021; 116: 515-523https://doi.org/10.21614/chirurgia.116.5.515
        • Fiorentino E.
        The consumption of snacks and soft drinks between meals may contribute to the development and to persistence of gastro-esophageal reflux disease.
        Med Hypotheses. 2019; 125: 84-88https://doi.org/10.1016/j.mehy.2019.02.034
        • Zubcic Z
        • Mendes T
        • Vceva A
        • et al.
        Presence of pepsin in laryngeal tissue and saliva in benign and malignant neoplasms.
        Biosci Rep. 2020; 40https://doi.org/10.1042/BSR20200216
        • Lechien J R
        • Bobin F
        • Dequanter D
        • et al.
        Does Pepsin Saliva Concentration (Peptest) Predict the Therapeutic Response of Laryngopharyngeal Reflux Patients?.
        Ann Otol Rhinol Laryngol. 2021; 3489420986347https://doi.org/10.1177/0003489420986347
        • Dodds W J
        • Hogan W J
        • Reid D P
        • et al.
        A comparison between primary esophageal peristalsis following wet and dry swallows.
        J Appl Physiol. 1973; 35: 851-857https://doi.org/10.1152/jappl.1973.35.6.851
        • Dent J
        • Dodds W J
        • Friedman R H
        • et al.
        Mechanism of gastroesophageal reflux in recumbent asymptomatic human subjects.
        J Clin Investig. 1980; 65: 256-267https://doi.org/10.1172/jci109667
        • Bobin F
        • Journe F
        • Lechien J R
        Saliva pepsin level of laryngopharyngeal reflux patients is not correlated with reflux episodes.
        Laryngoscope. 2020; 130: 1278-1281https://doi.org/10.1002/lary.28260
        • Johnston N
        • Wells C W
        • Samuels T L
        • et al.
        Pepsin in nonacidic refluxate can damage hypopharyngeal epithelial cells.
        Ann Otol Rhinol Laryngol. 2009; 118: 677-685https://doi.org/10.1177/000348940911800913
        • Kahrilas P J
        • Gupta R R
        The effect of cigarette smoking on salivation and esophageal acid clearance.
        J Lab Clin Med. 1989; 114: 431-438
        • Lechien J R
        • Bobin F
        • Muls V
        • et al.
        Saliva pepsin concentration of laryngopharyngeal reflux patients is influenced by meals consumed before the samples.
        Laryngoscope. 2021; 131: 350-359https://doi.org/10.1002/lary.28756
        • Bulmer D M
        • Ali M S
        • Brownlee I A
        • et al.
        Laryngeal mucosa: its susceptibility to damage by acid and pepsin.
        Laryngoscope. 2010; 120: 777-782https://doi.org/10.1002/lary.20665
        • Johnston N
        • Wells C W
        • Blumin J H
        • et al.
        Receptor-mediated uptake of pepsin by laryngeal epithelial cells.
        Ann Otol Rhinol Laryngol. 2007; 116: 934-938https://doi.org/10.1177/000348940711601211
        • Johnston N
        • Dettmar P W
        • Bishwokarma B
        • et al.
        Activity/stability of human pepsin: implications for reflux attributed laryngeal disease.
        Laryngoscope. 2007; 117: 1036-1039https://doi.org/10.1097/MLG.0b013e31804154c3
        • Park W
        • Hicks D M
        • Khandwala F
        • et al.
        Laryngopharyngeal reflux: prospective cohort study evaluating optimal dose of proton-pump inhibitor therapy and pretherapy predictors of response.
        Laryngoscope. 2005; 115: 1230-1238https://doi.org/10.1097/01.Mlg.0000163746.81766.45
        • Lechien J R
        • Bobin F
        • Dapri G
        • et al.
        Hypopharyngeal-Esophageal Impedance-pH Monitoring Profiles of Laryngopharyngeal Reflux Patients.
        Laryngoscope. 2021; 131: 268-276https://doi.org/10.1002/lary.28736