Possible association between Helicobacter pylori infection and vocal fold leukoplakia

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1 Received: 23 September 2017 Revised: 6 November 2017 Accepted: 26 January 2018 DOI: /hed ORIGINAL ARTICLE Possible association between Helicobacter pylori infection and vocal fold leukoplakia Min Chen MD 1,2 Jian Chen MD 1,2 Yue Yang MD 1,2 Lei Cheng MD 1,2 Hai-Tao Wu MD 1,2 1 Department of Otolaryngology - Head and Neck Surgery, Eye, Ear, Nose, and Throat Hospital, Fudan University, Shanghai, China 2 Shanghai Key Clinical Disciplines of Otorhinolaryngology, Shanghai, China Correspondence Haitao Wu, Department of Otolaryngology - Head and Neck Surgery, Eye, Ear, Nose, and Throat Hospital of Fudan University, 83 Fenyang Road, Shanghai, China, eentwuhaitao@163.com Funding information This study was funded by grant no from the Science and Technology Commission of Shanghai Municipality of China and grant no. 2016LP019 from the Traditional Chinese Medicine scientific research of Health and Family Planning Commission of Shanghai Municipality of China Abstract Background: Several studies have indicated the larynx as possible Helicobacter pylori (H. pylori) reservoirs. This study explored the association between H. pylori and vocal fold leukoplakia. Methods: The case-control study involved 51 patients with vocal fold leukoplakia and 35 control patients with vocal polyps. Helicobacter pylori was detected in tissues by the rapid urease test, nested polymerase chain reaction (PCR), and single-step PCR. The H. pylori-specific immunoglobulin antibodies were detected in plasma by enzyme-linked immunosorbent assay (ELISA). Results: Helicobacter pylori-positive rate of vocal fold leukoplakia and vocal polyps was 23.5% versus 11.4% (P 5.157), 37.2% versus 14.3% (P 5.020), 27.5% versus 8.6% (P 5.031), and 70.6% versus 68.6% (P 5.841) detected by rapid urease test, nested PCR, single-step PCR, and ELISA, respectively. Regression analysis indicated that H. pylori infection (P 5.044) was the independent risk factor for vocal fold leukoplakia. Conclusion: Helicobacter pylori infection exists in the larynx and may be associated with vocal fold leukoplakia. KEYWORDS Helicobacter pylori, laryngopharyngeal reflux, leukoplakia, polyps, vocal fold 1 INTRODUCTION Vocal fold leukoplakia is a clinical diagnosis indicating abnormal white patches or plaques on the vocal mucosa that cannot be classified clinically as any other condition. 1 Histopathological changes based on a 5-grade dysplasia system, which is most widely used showing keratosis or dyskeratosis accompanied by hyperplasia with non-dysplasia, mild dysplasia, moderate dysplasia, severe dysplasia, or carcinoma. 2 Vocal fold leukoplakia is often considered to be a precancerous condition of laryngeal squamous cell carcinoma (SCC) This work was presented at the Department of Otolaryngology - Head and Neck Surgery, Eye, Ear, Nose, and Throat Hospital of Fudan University, 83 Fenyang Road, Shanghai, China. and portents a risk of malignant transformation with 8%. 3 Tobacco and alcohol abuse remain the major risk factors with laryngopharyngeal reflux (LPR) recently considered as a possible factor. 4 Recent studies of vocal fold leukoplakia have been devoted to genetic changes, such as TP53, P16, matrix metalloproteinase (MMP)-1, MMP-2, and MMP-3. 5,6 On the contrary, there is little evidence that microbiological agents are involved in pathogenesis for vocal fold leukoplakia. Helicobacter pylori (H. pylori), a gram-negative spiral bacterium, is an important microbiological pathogen for humans, associated with a substantial burden from both malignant and nonmalignant diseases. 7 The pathogenicity of H. pylori in gastrointestinal lesions has been extensively studied, recently, the role of this bacterium in rhinitis, 1498 VC 2018 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/hed Head & Neck. 2018;40:

2 CHEN ET AL FIGURE 1 A, Positive and B, negative rapid urease test results for diagnosis of Helicobacter pylori in patients with vocal fold leukoplakia, where the indicator changed the color of media from yellow to blue within 60 minutes [Color figure can be viewed at wileyonlinelibrary.com] adenoiditis, tonsillitis, otitis media, pharyngeal diseases, and laryngeal diseases has been investigated. 8 In the literature on benign and malignant laryngeal disorders, the relative importance of H. pylori has been subject to considerable discussion It has been also detected in the oral leukoplakia. 11 However, no previous study has investigated H. pylori infection and vocal fold leukoplakia. Various detection methods for H. pylori have been developed, which might contribute to controversial results on the role of H. pylori for laryngeal disease. Noninvasive tests, such as the urea breath test and serology by enzyme-linked immunosorbent assay (ELISA), are usually preferred by the clinicians. Invasive tests involving the rapid urease test, polymerase chain reaction (PCR), histology, and culture are also available. 12 Each of them has one or more advantages or disadvantages. Nonetheless, the nested PCR-based technique, if performed properly, could be proposed as the gold standard test. 13,14 The purpose of this study was to investigate whether H. pylori can colonize in the vocal folds of patients with vocal fold leukoplakia. It is the first study to determine the relationship between H. pylori infection and vocal fold leukoplakia. We designed a case-control study, used the rapid urease test, nested PCR, and single-step PCR to detect H. pylori infection in the tissues and ELISA to detect antibodies against H. pylori in the plasma. 2 MATERIALS AND METHODS 2.1 Patients A case-control study that included 86 patients admitted into the Department of Otolaryngology - Head and Neck Surgery, Eye, Ear, Nose, and Throat Hospital of Fudan University in Shanghai was conducted during March 2016 to July The protocol of this study was approved by the Institutional Review Board of the Eye, Ear, Nose, and Throat Hospital of Fudan University. Written informed consent was obtained from each participant. The case group was composed of 51 patients with vocal fold leukoplakia who were clinically visualized as having an abnormal white mucosal lesion on the vocal fold by rigid or flexible laryngoscopy and pathologically diagnosed as keratosis or dyskeratosis with hyperplasia, non-dysplasia, dysplasia, or carcinoma in situ. The control group was composed of 35 patients with vocal polyps confirmed by postoperative pathology.

3 1500 CHEN ET AL. The exclusion criteria for both patients in the case group and the control group were the diagnosis of chronic gastritis, peptic ulcer disease, or gastric cancer, prior to taking of antibiotics or bismuth for 4 weeks, proton pump inhibitors, or H 2 receptor antagonists for 2 weeks, and a history of immune compromise, with the use of steroids during the previous 3 months. Also excluded were patients who underwent radiotherapy or blood transfusions within the previous 6 months. 2.2 Clinical data Clinical data, including age, sex, smoking history, alcohol consumption, LPR, laryngoscopic images, and pathological results were collected. Subjects were classified as smokers and nonsmokers according to smoking history. Smokers, including former smokers (having not smoked for at least 12 months) and current smokers, nonsmokers defined as patients with no history of smoking or having not smoked for at least 10 years. Depending on alcohol consumption, subjects were divided into drinkers (with consumption of >80 ml of pure alcohol per day) and nondrinkers. Drinkers were further grouped as former drinkers (having not drunk for at least 12 months) and current drinkers. Smoking index was calculated as the number of cigarettes consumed per day multiplied by years of smoking. The drinking index was calculated as the volume of pure alcohol consumed per day multiplied by years of drinking. The LPR was diagnosed based on the scores of the Reflux Symptom Index (RSI) chart. 15 Pathological results of vocal fold leukoplakia were based on the 5-grade dysplasia system and the 2-grade dysplasia system. 16 The size of vocal fold leukoplakia was graded as <50% (the sum of all leukoplakia is less than half the length of one entire vocal fold) or 50% (the sum of all leukoplakia is more than half the length of one entire vocal fold). 2.3 Sample collection Each laryngeal tissue sample obtained during the suspension microlaryngoscopy was divided into 3 parts, the first for routine pathological examination, the second for the rapid urease test, and the last for PCR. Plasma samples were separated from blood drawn aseptically by venipuncture. The tissue specimens for PCR and plasma for each patient were stored at 2808C. 2.4 Rapid urease test The Pyloritek test kit (Serim Research Corporation, Elkhart, IN) contains substrate urea and a PH indicator (bromophenol blue). The ammonia produced is detected with the PH indicator, which turns from yellow to blue at an elevated PH. Laryngeal tissue for the rapid urease test was separated into 2 parts and pushed from the forceps directly onto the kit with a clean wooden applicator stick, in accord with the FIGURE 2 Amplification of A, partial 501bp HSP60 gene and B, 294bp UreC gene for Helicobacter pylori in vocal fold leukoplakia (lanes 1-6) and vocal polyps (lanes 7-10). M, 2000bp DNA marker A, 500bp DNA marker B; lane 11 5 positive control and lane 12 5 negative control manufacturer s instructions. Within 60 minutes, we observed the upper right-hand corner of the yellow reaction pad to confirm the appearance of the intense blue positive control spot. A similar color over one of the specimens indicates that the specimen is infected with H. pylori. The appearance of a pale blue or faint gray haze over the specimen at 60 minutes is considered a negative result (see Figure 1). 2.5 Nested polymerase chain reaction and single-step polymerase chain reaction Genomic DNA extraction from tissues was carried out using a QIAamp DNA Mini kit (QIAGEN, Hilden, Germany) followed by nested PCR for the HSP60 gene and single-step PCR for the UreC gene. The PCR was carried out in a 15 ll volume using 60 ng of DNA, ll of Taq polymerase (Takara, Dalian, China), and 0.2 mm of each primer (Sangon, Shanghai, China), 0.25 mm (each) deoxynucleotide triphosphate (Takara, Dalian, China), and 2 mm MgCl 2,and1lL of the PCR product from the primary cycle was used as the template in the nested PCR. Primers of the HSP60 gene carried out by nested PCR were as follows; primer-1(5 0 AAGGCATGCAATTTGATAGAGGCT 3 0 ), primer-2(5 0 CTTTTTTCTCTTTCATTTCCACTT 3 0 ), primer-3(5 0 TT GATAGAGGCTACCT CTCC 3 0 ), and primer-4(5 0 TGT CATAATCGCTTGTCGTGC 3 0 ). The amplification reaction for both primary and nested cycles comprised initial melting

4 CHEN ET AL TABLE 1 Clinical characteristics and Helicobacter pylori infection detected by 4 methods within the case and control groups Cases Controls No. of patients No. of patients (%) No. of patients No. of patients (%) P value Sex Male Female Age, years < < Smoking Smokers Former Current Nonsmokers Drinking Drinkers Former Current Nondrinkers a.176 b LPR.359 Yes No Rapid urease test.157 Positive Negative Nested PCR.020 Positive Negative Single-step PCR.031 Positive Negative ELISA.841 Positive Negative Abbreviations: ELISA, enzyme-linked immunosorbent assay; LPR, laryngopharyngeal reflux; PCR, polymerase chain reaction. a Smokers vs nonsmokers. b Drinkers vs nondrinkers. at 958C for 5 minutes, which was followed by 34 cycles of 30 seconds at 948C, 30 seconds at 568C, and 728C for30 seconds with a final extension step of 10 minutes at 728C. The final PCR product was 501 bp. Primers of the UreC gene carried out by single-step PCR were as follows; primer-1(5 0 AAGCTTTTAGGGGTGTTAGGGGTT 3 0 ), and primer-2(5 0 AAGCTTACTTTCTAACACTAACGC 3 0 ). The amplification reaction comprised initial melting at 958C for 5 minutes, which was followed by 36 cycles of 30 seconds at 948C, 30 seconds at 568C, and 728C for 30 seconds with a final extension step of 10 minutes at 728C. The expected PCR product was 294 bp. All the amplifications were carried out in a thermal cycler (Bio-Rad, Hercules, CA). DNA from H. pylori reference (ATCC 26695) and a sample without DNA were assayed in each PCR run as positive and negative controls, respectively. To identify the amplified products, 10 ll of the PCR product was analyzed by electrophoresis on 2% agarose gels

5 1502 CHEN ET AL. association between H. pylori infection and characteristics of vocal fold leukoplakia was compared by univariate analysis. We used the Student s t test for continuous variables and Pearson chi-square test or Fisher s exact test for binary variables in univariate analysis. A 2-tailed P value <.05 was considered statistically significant. 3 RESULTS FIGURE 3 Receiver operating characteristic analysis and the areas under the curve of single-step polymerase chain reaction (PCR), rapid urease test (RUT), enzyme-linked immunosorbent assay (ELISA), and laryngopharyngeal reflux (LPR) for identified Helicobacter pylori infection at 100V with 1*TAE buffer. The Genegreen-stained DNA in the gels was visualized in an ultraviolet transilluminator box (Peiqing Science and Technology, Shanghai, China), as shown in Figure Enzyme-linked immunosorbent assay Plasma samples of both study and control groups were evaluated for H. pylori-specific immunoglobulin antibodies by ELISA kit (Demeditec, Dusseldorf, Germany), in accord with the manufacturer s instructions. 2.7 Statistical analysis All statistical tests were performed using SPSS version 20.0 (IBM, Chicago, IL). Clinical parameters and H. pylori infection detected by 4 methods, respectively, within case and control groups were examined by univariate analysis. Based on the detective results from nested PCR, multivariate logistic regression models were applied to assess possible risk factors. The diagnostic accuracy of these detection methods for H. pylori was evaluated using the area under the receiver operating characteristics (ROC) curve analysis. The Of the 86 patients included in this study, 51 cases were vocal fold leukoplakia and 35 cases were vocal polyps. The baseline characteristics of the patients and H. pylori infection detected by 4 methods are shown in Table 1. Analyzed by Student s t test, age, smoking index, and alcohol index for cases versus control were versus (P <.001), versus (P 5.013), and versus (P 5.129), respectively. According to univariate analysis, the male:female ratio and age were significantly different between the case and control groups. Prevalence of smoking and smoking index were significantly higher among cases than among controls. There was no statistically significant difference in alcohol consumption and LPR. The H. pylori-positive rate of vocal fold leukoplakia and vocal polyps was 23.5% versus 11.4% (P 5.157), 37.3% versus 14.3% (P 5.020), and 27.5% versus 8.6% (P 5.031) detected in tissues by rapid urease test, nested PCR, and single-step PCR, respectively. The H. pylori-specific antibodies were detected in 70.6% of the patients with vocal fold leukoplakia and 68.6% of the patients with vocal polyps in blood samples by ELISA (P 5.841; Table 1). Based on the diagnostic results of H. pylori infection determined by nested PCR, the ROC curve analysis of the rapid urease test, single-step PCR, ELISA, and LPR are presented in Figure 3. The area under the curve for the rapid urease test, single-step PCR, ELISA, and LPR were (95% confidence interval [CI] ; P 5.022), (95% CI ; P <.001), (95% CI ; P 5.078), and (95% CI ; P 5.018), respectively. TABLE 2 Multivariate logistic regression analysis of risk factors for vocal fold leukoplakia Factors Odds ratio 95% CI P value Sex, male vs female Age, years, <60 vs <.001 Smoking, smokers vs nonsmokers H. pylori infection, a positive vs negative Abbreviations: CI, confidence interval; H. pylori, Helicobacter pylori. a H. pylori infection was tested by nested polymerase chain reaction.

6 CHEN ET AL TABLE 3 Comparison of clinical characteristics in vocal fold leukoplakia with and without Helicobacter pylori infection H. pylori positive H. pylori negative No. of patients % No. of patients % P value Sex.373 Male Female Age, years.973 < Smoking Smokers Former Current Nonsmokers Drinking Drinkers Former Current Nondrinkers a.838 b LPR.036 Yes No Size of lesion.213 <50% % Site of lesion.945 Unilateral Bilateral Pathological grade Low-grade No dysplasia Mild dysplasia High-grade Moderate Severe Carcinoma in situ c Abbreviations: H. pylori, Helicobacter pylori; LPR, laryngopharyngeal reflux. a Smokers vs nonsmokers. b Drinkers vs nondrinkers. c Low-grade vs high-grade. The H. pylori infection identified by nested PCR and other parameters with significant values in univariate analysis were fitted into multivariate logistic regression analysis (Table 2). Age (P <.001) and H. pylori infection (P 5.044) were identified as independent risk factors associated with vocal fold leukoplakia. The results of stratified analysis were consistent with the multivariate logistic regression analysis (Supporting Information Table S1). The 51 cases of vocal fold leukoplakia were divided into 2 groups based on the presence or absence of H. pylori identified by nested PCR. Demographic and clinical characteristics were compared between these 2 groups (Table 3). Statistical analysis revealed that LPR was associated with the presence of H. pylori in the vocal fold leukoplakia (42.1% vs 15.6%; P 5.036). An association was also observed between pathological grade and the presence of the H. pylori

7 1504 CHEN ET AL. (10.6% vs 89.4%; P 5.028). Patient s sex, age, tobacco use, alcohol consumption, size of lesion, site of lesion, and morphological type of vocal fold leukoplakia did not correlate with the presence of H. pylori. 4 DISCUSSION Risk factors, including tobacco use, alcohol consumption, voice abuse, LPR, and inflammation, have been regarded as etiologies causing a transition from normal epithelium to dysplasia or SCC of the larynx. 1,4 However, the definite role of these factors on vocal fold leukoplakia is still unknown. Compared to the control group, vocal fold leukoplakia showed a distinct male and advanced age predisposition in this study, which is similar to various studies. 1,17 Although smoking might be not an independent risk factor for vocal fold leukoplakia, combined with other factors it should be highlighted. Additionally, the significant higher smoking index was observed in the case group. Therefore, the environmental and lifestyle-related chronic accumulative stimulation, especially tobacco exposures, should not be negligible for pathogenesis of vocal fold leukoplakia. To our knowledge, this is the first study to describe whether or not H. pylori is present in vocal fold leukoplakia. The existence of H. pylori in the vocal fold leukoplakia was proven by rapid urease test, nested PCR, and single-step PCR (Figures 1 and 2). Although a specific correlation between H. pylori and upper aerodigestive tract diseases has not been established, the presence of H. pylori in the upper aerodigestive tract is more and more accepted. 8,18 Siupsinskiene et al 9 reported that H. pylori can colonize in the larynx of patients with vocal polyps, laryngitis, vocal nodules, and laryngeal carcinoma. As noted by Fellmann et al, 19 H. pylori was found in 38% of the tissues from the larynx, pharynx, and oral cavity, where seems to be an additional reservoir for this bacterium. The outcome of this study further supported the idea of the existence of H. pylori in the larynx. Furthermore, one of the purposes of this study was to determine the role of H. pylori for the patients with vocal fold leukoplakia. The H. pylori infection identified by nested PCR was significant in both univariate and multivariate analysis comparing with control subjects (Tables 1 and 2), indicating that H. pylori might be a risk factor for vocal fold leukoplakia. Literature data revealed that H. pylori was not considered a normal microflora in healthy laryngeal mucosa. 20 A possible pathogenesis of vocal fold leukoplakia has been explained by the inflammation induced by this bacterium leading to epithelial cell proliferation. The potential for destroying epithelial mucosa and inflammation could cause chronic injury resulting in larynx pathology. 21,22 The H. pylori has been studied thoroughly in the last 2 decades to explore possible links to benign and malignant laryngeal lesions. 4 To date, there was no evidence that H. pylori was involved in pathogenesis for vocal fold leukoplakia. Several studies have maintained H. pylori as a risk factor in laryngeal SCC, but other studies disagree These discrepant results might depend on the various detection methods for H. pylori, the incidence of H. pylori infection in the general population, and subject inclusion criteria. In the current study, a highly conserved gene, HSP60, was targeted to identify H. pylori by nested PCR, which has been proposed as the gold standard test. 13,27 There was a higher positive rate of H. pylori detected by nested PCR compared with the single-step PCR and rapid urease tests, in line with the previous study. 14 Fang et al 28 and Siupsinskiene et al 9 found that 39.4% and 32% of vocal polyps cases were H. pylori-positive using the rapid urease test, respectively. Although, in our study, we discovered a low H. pylori-positive rate of 11.4% in vocal fold polyp. A possible reason might be the PH indicator we used was bromophenol blue, which can be distinguished from the confusing coloration of blood on tissue for visual judgement, compared to the red indicator used in previous studies mentioned above. 9,28 Even though these methods all have reference values for diagnosis of H. pylori infection, the target gene in tissues detected by PCR was recommended according to the ROC analysis (see Figure 3). These tests seem to be sensitive enough only when the density of H. pylori remains high. The PCR-based technique can detect even a few bacteria. Diagnostic results, especially the results of serology, also varied with the prevalence of H. pylori infection. 12 Developed countries tend to have lower general prevalence than developing countries. 7 In the present study, no significant difference was discovered for H. pylori antibodies by ELISA among the study and control groups. The H. pylori-positive rate was generally higher based on measuring immunoglobulin antibodies because it did not discriminate between current and former infections. 12,19 In order to avoid the confounding factors, we excluded those patients who were diagnosed with chronic gastritis, peptic ulcer disease or gastric cancer, have taken antibiotics or bismuth for 4 weeks, proton pump inhibitors, or H 2 receptor antagonists for 2 weeks, which might also lead to the lower H. pylori-positive rate than other studies. 9,23,28 Approximately 50% of the high-grade vocal fold leukoplakia contained this organism, revealing the relationship between pathological grade and the presence of the H. pylori. Other features, including patient s sex, age, tobacco use, alcohol consumption, size of lesion, and site of lesion of vocal fold leukoplakia, were not associated with the presence of the H. pylori. It became firmly established as a major human carcinogen. The infection causing persistent chronic gastritis has been extensively studied, which for individuals

8 CHEN ET AL might develop from metaplasia, mild dysplasia, moderate dysplasia, severe dysplasia, and eventually gastric tumors by arising endogenous DNA damage and increasing mucosa dysfunction in gastric epithelial. 21,29 Even with quite a few literatures highlighting the relationship between H. pylori infection and laryngeal SCC, the precise mechanism how this bacterium worked in the process of laryngeal SCC is still lacking. Long-term exposure to H. pylori infection was associated with progression of precancerous lesions. 30 Higher H. pylori-positive rates of vocal fold leukoplakia with highdegree dysplasia suggested that similar mechanisms for gastric premalignant lesions and carcinoma might also be performed in the occurrence and progression of vocal fold leukoplakia. Further work focusing the role of H. pylori in leukoplakia is strongly recommended. More information on this matter would help us to establish a greater degree of accuracy on the connection between H. pylori and laryngeal disease. Recently, the role of LPR for vocal fold leukoplakia was under debate. In the current study, LPR was found in 25.5% of the vocal fold leukoplakia cases. No significant correlation was observed between LPR and vocal fold leukoplakia. Healthy laryngeal tissues from the healthy group could not be obtained in this study due to the medicolegal aspects. The control samples included were vocal polyps, which was suggested to be a relation with LPR. 31 With the diagnosis of LPR by RSI, Rafii et al 32 pointed out that LPR may be overdiagnosed and other etiologies must be considered for patients with hoarseness, including vocal fold leukoplakia. Li et al 33 conducted an ambulatory 24-hour multichannel intraluminal impedance-ph monitoring study to conclude that there was no significant difference in the reflux event between vocal fold leukoplakia and normal control. On the contrary, Gong et al 34 used pepsin as a biomarker and identified the incidence of vocal fold leukoplakia associated with LPR. Therefore, combined methods should be applied for detecting the existence of LPR. Additionally, H. pylori infection in vocal fold leukoplakia has been found more frequently in patients with LPR (Table 3). The ROC curve analysis also indicated a reference value of LPR for determining H. pylori infection. The presence of H. pylori showed a link with LPR, corroborating the data obtained in a meta-analysis. 35 A recent finding showed a positive relationship between H. pylori and LPR signs assessed by the Reflux Finding Score. 36 The mode of transmission of this bacterium to the upper airway has been described. 8,21 These findings support the hypothesis that the episodes of LPR may play an important role in the transmission of H. pylori into the larynx. However, considerably more work will need to be done to confirm these issues. This study, however, has limitations. First, for the type of epidemiological study, a larger sample size should be included in this study. Second, healthy laryngeal tissues cannot be taken as normal control because of ethical and medicolegal aspects. Third, LPR was only diagnosed based on the scores of the RSI chart. The multidisciplinary cooperation is required to establish the diagnosis of LPR by combined methods. Long-term follow-up was also needed for patients with vocal fold leukoplakia to determine whether or not H. pylori infection was associated with recurrence or malignant transformation of vocal fold leukoplakia. 5 CONCLUSION This study supported that H. pylori was present in the mucosa of the larynx. It was reported for the first time that H. pylori may be the independent risk factor for vocal fold leukoplakia. Furthermore, H. pylori presence in the vocal fold leukoplakia was related to the pathological grades. In addition, there exists an association between the presence of H. pylori and episodes of LPR. The described findings indicate that further studies with larger sample sizes on the precise mechanisms of how this bacterium works is necessary. CONFLICT OF INTEREST The authors declare that they have no conflict of interest. FUNDING INFORMATION The study was funded by grant no from the Science and Technology Commission of Shanghai Municipality of China and grant no. 2016LP019 from the Traditional Chinese Medicine scientific research of Health and Family Planning Commission of Shanghai Municipality of China. ETHICAL APPROVAL All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. INFORMED CONSENT Informed consent was obtained from all individual participants included in the study. ORCID Hai-Tao Wu MD

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10 CHEN ET AL early glottic cancer]. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2014;49: [34] Gong X, Wang XY, Yang L, Sun MJ, Du J, Zhang W. Detecting laryngopharyngeal reflux by immunohistochemistry of pepsin in the biopsies of vocal fold leukoplakia. J Voice [35] Campbell R, Kilty SJ, Hutton B, Bonaparte JP. The Role of Helicobacter pylori in laryngopharyngeal reflux. Otolaryngol Head Neck Surg. 2017;156: [36] Siupsinskiene N, Katutiene I, Jonikiene V, Janciauskas D, Vaitkus S. Helicobacter pylori in the tonsillar tissue: a possible association with chronic tonsillitis and laryngopharyngeal reflux. J Laryngol Otol. 2017;131: SUPPORTING INFORMATION Additional Supporting Information may be found online in the supporting information tab for this article. How to cite this article: Chen M, Chen J, Yang Y, Cheng L, Wu H-T. Possible association between Helicobacter pylori infection and vocal fold leukoplakia. Head & Neck. 2018;40: /hed.25121

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