Abstract
Background
We investigated the relationship between Laryngopharyngeal Reflux (LPR) and maxillary sinus mucosal thickness (MSMT), inferior turbinate mucosal thickness (ITMT), inferior turbinate width (ITW) and nasal septal body thickness (NSBT), which can be signs of chronic rhinosinusitis and allergic rhinitis.
Methods
The study, which included 87 patients, was designed as two groups. While 42 of the patients were included in the Laryngopharyngeal Reflux group, 45 were included in the control group. Age and gender information of the patients were noted. MSMT, ITMT, ITW and NSBT values were measured in patients who had Paranasal Sinus Computed Tomography. MSMT, ITMT and ITW were measured as right and left. Both groups were evaluated in terms of these values.
Results
Right ITMT, bilateral ITW and MSMT values were found to be significantly higher in the LPR group than in the control group (p < 0.05). MSMT values were higher in males (p < 0.05). The left-ITT and NSBT values were not significantly different between the LPR group and the control group, but both values were higher in the LPR group than in the control group (p > 0.05). In the LPR group, there were positive correlations between ITMT and ITW values of the right side; and left side separately (p < 0.05).
Conclusion
It has been shown that Laryngopharyngeal Reflux increases maxillary sinus mucosal thickness, inferior turbinate thickness and width, and nasal septal body thickness, which can be signs of chronic rhinosinusitis and allergic rhinitis. The negative effects of LPR on nasal and paranasal mucosa and structures were demonstrated in this study.
Keywords: Inferior turbinate, Laryngopharyngeal reflux, Maxillary sinus, Nasal septal body, Paranasal Sinus Computed Tomography
Introduction
Laryngopharyngeal Reflux (LPR), described by Cherry and Margulies in 1968, causes nonspecific symptoms such as cough, hoarseness, globus pharyngeus, oropharyngeal secretion and frequent throat clearing [1]. It is difficult to diagnose because it causes too many nonspecific symptoms. The 24-hour double-probe pH monitoring test can objectively detect reflux of gastroesophageal contents into the upper respiratory tract. Reflux Symptom Index (RSI) suggested by Belafsky et al. and Reflux Significant Score (RFS) evaluated by videolaryngoscopic examination are subjective methods used in diagnosis [2, 3]. RSI above 13 is considered pathological, while RBS above 7 is in favour of LPR.
Many acute and chronic factors such as upper respiratory tract infections, immunodeficiency, asthma and irritant inhalers cause inflammation in the maxillary sinus mucosa [4, 5]. Nasal Septal Body (NSB), an erectile tissue, is located in front of the inferior turbinate and above the middle turbinate. It is thought to provide additional resistance to nasal airflow. Inferior turbinate (IT) is the turbinate whose volume changes the most. Mucosal thickness changes in many acute and chronic diseases, especially in allergic rhinitis.
In this study, we aimed to show the changes in nasal structures due to chronic inflammation resulting from LPR with the thickness of the maxillary sinus mucosa, nasal septal body and inferior turbinate mucosa; and inferior turbinate width.
Materials and Methods
This retrospective study was conducted in Kırıkkale University Faculty of Medicine, Departments of Radiology and Otorhinolaryngology, according to the principles of Declaration of Helsinki. Paranasal Sinus Computed Tomography records were obtained from the Kırıkkale University Faculty of Medicine Radiology Department database. Ethics committee approval was obtained from the Non-invasive Researches Ethics Committee of Kırıkkale University (Date: 27.04.2022, Number: 2022.04.21).
Subjects
In this retrospective study, 102 patients who applied to the Ear, Nose and Throat outpatient clinic between January and April 2022 were screened. After exclusion of patients with nasal symptoms or nasal disease, 87 eligible patients were included in the study. Forty-two patients diagnosed with LPR were divided into Group 1 and 45 patients without additional pathology in Paranasal Sinus Computed Tomography (PNSCT) were divided into Group 2 (control group).
Age and gender distribution of the patients were obtained. The PNSCT of the patients diagnosed with LPR according to physical examination and RSI and RFS in the last 3 months was scanned. PNSCT images (Multi-slice CT-MSCT) were obtained from the digital archive of the … Faculty of Medicine Radiology Department. Patients under the age of 18 years and older than 60 years, patients with nasal complaints, patients who have had surgery or trauma from the sinonasal region, allergic rhinitis, acute or chronic sinusitis, patients with nasal polyposis, using nasal medication and patients with benign or malignant tumors were excluded from the study.
CT Imaging and Measurements
All of the scans were obtained with routine PNS computed tomography imaging in the supine position, without contrast. The images were acquired using a 64-slice CT (MSCT; Brilliance 64, Philips Medical System, Best, the Netherlands). All of the scans were obtained using the following parameters: tube volt age 120 kV, effective mAs 350, slice thickness 1.00 mm, field of view (FOV) 180 mm and image matrix 768 × 768. The images were transferred to a workstation and the raw data were reconstructed using bone algorithms. After scanning, the coronal, axial and sagittal images were reconstructed with a slice thickness of 1.00 mm. The coronal plan was preferred for measurements.
The same radiologist with more than 12 years of experience in radiology, performed all the measurements on a high-resolution monitor. All measurements were recorded in millimeters (mm):
1- Nasal Septal Body thickness (NSBT) were determined the according to previous studies [6]. The measurement was made from the section where the nasal septal was thickest in the coronal plane (Fig. 1).
Fig. 1.
On coronal image, nasal septal body thickness is measured at maximum visible section as millimeters
2-For Inferior turbinate mucosal thickness (ITMT), the widths of the right and left inferior turbinates (ITW), which are the most prominent images in the coronal section, were measured (Fig. 2).
Fig. 2.
On the coronal section, the width of the inferior turbinates are measured at maximum visible section as millimeters
3-Right and left mucosal thickening in the maxillary sinus (MSMT) was measured at the thickest point in the coronal section (Figure-3). Sinus retention cysts and fluid levels were excluded from measurements.
Fig. 3.
On coronal image left mucosal thickening in the maxillary sinus is measured at the thickest point as millimeter
Statistical Analysis
SPSS Statistics 24.0 (IBM SPSS Inc, Chicago) program was used for statistical analysis. The Chi-square test, Paired Sample t test, Mann Whitney U test, Independent samples t test, Paired samples-t test, Mann-Whitney U test, Wilcoxon Signed Ranks test, Pearson correlation test and Spearman’s correlation rho efficient testwere used.
A value of p<0.05 was considered statistically significant.
Results
Demographic features of the patients are given in Table 1. There was no significant difference between the two groups in terms of age (p = 0.37) and gender (p = 0.54) (Table 1).
Table 1.
Demographic features of patients
| Group 1 (LPR) (n = 42) |
Group 2 (Control) (n = 45) | p values | |
|---|---|---|---|
| Age (years) | 35.09 ± 13.55 | 32.48 ± 10.88 | 0.37* |
|
Gender • Female • Male |
21 (50.0%) 21 (50.0%) |
22 (48.9%) 23 (51.1%) |
0.54¥ |
*: Mann-Whitney U test was used. ¥: Chi-square test was used. Data represent mean ± SD excluding threshold values. LPR, Laryngopharyngeal Reflux
Inferior turbinate mucosal thickness (ITMT) and width (ITW), maxillary sinus mucosal thickness (MSMT), and nasal septal body thickness (NSBT) values of the groups were shown on Table 2.
Table 2.
Inferior turbinate mucosal thickness and width, maxillary sinus mucosal thickness, and nasal septal body thickness values of the groups
| Group 1 (LPR) (n = 42) |
Group 2 (Control) (n = 45) |
p values** | ||
|---|---|---|---|---|
| Inferior Turbinate Mucosal Thickness (mm) | R | 10.00 ± 3.02 | 8.51 ± 2.16 | 0.010 |
| L | 9.68 ± 2.41 | 8.40 ± 2.40 | 0.160 | |
| P** | 0.276 | 0.201 | ||
| Inferior Turbinate Width (mm) | R | 10.00 ± 3.02 | 8.51 ± 2.16 | 0.009 |
| L | 9.68 ± 2.41 | 8.40 ± 2.40 | 0.016 | |
| P** | 0.573 | 0.826 | ||
| Maxillary Sinus Mucosal Thickness (mm) | R | 3.23 ± 1.68 | 1.30 ± 1.06 | < 0.001 |
| L | 2.85 ± 2.41 | 1.12 ± 1.08 | < 0.001*** | |
| P**** | 0.104 | 0.372 | ||
| Nasal Septal Body Thickness (mm) | 10.29 ± 1.85 | 9.80 ± 1.71 | 0.210 | |
*Independent samples-t test was used
**Paired samples-t test was used
***Mann-Whitney U test was used
****Wilcoxon signed ranks test was used
Data represent mean ± SD excluding threshold values. LPR, Laryngopharyngeal Reflux
Inferior Turbinate Mucosal Thickness (ITMT)
Right ITMT values of the LPR group were significantly higher than those of the control group (p < 0.05). In each of the groups separately, there were no significant differences between ITMT values of the right and left sides (p > 0.05) (Table 2).
Inferior Turbinate Width (ITW)
Bilateral ITW values of the LPR group were significantly higher than those of the control group (p < 0.05) (Table 2). In each of the groups separately, there were no significant differences between ITW values of the right and left sides (p > 0.05) (Table 2).
Maxillary Sinus Mucosal Thickness (MSMT)
Bilateral MSMT values of the LPR group were significantly higher than those of the control group (p < 0.05) (Table 2). In each of the groups separately, there were no significant differences between MSMT values of the right and left sides (p > 0.05) (Table 2).
Nasal Septal Body Thickness (NSBT)
There were no significant differences between the NSBT values of the groups (p > 0.05).
Correlation test results in LPR group were shown on Table 3: There were positive correlations between ITMT and ITW values of the right side; and left side separately (p < 0.05) (Table 3). In males, MSMT values were significantly higher than those in the females (p < 0.05) (Table 3).
Table 3.
Correlation test results in the LPR group (n = 42)
| ITMT (mm) | ITW (MM) | MSMT (mm) | NSBT(mm) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| R | L | R | L | R | L** | ||||
| ITMT (mm) | R | r | 0.302 | 0.837 | 0.111 | 0.073 | 0.046 | -0.019 | |
| P* | 0.052 | 0.000 | 0.482 | 0.646 | 0.770 | 0.907 | |||
| L | r | 0.302 | 0.214 | 0.710 | 0.003 | 0.156 | 0.138 | ||
| P* | 0.052 | 0.174 | 0.000 | 0.987 | 0.322 | 0.384 | |||
| ITW (mm) | R | r | 0.837 | 0.214 | 0.133 | 0.113 | -0.035 | -0.065 | |
| P* | 0.000 | 0.174 | 0.399 | 0.477 | 0.824 | 0.681 | |||
| L | r | 0.111 | 0.710 | 0.133 | 0.013 | 0.199 | 0.186 | ||
| P* | 0.482 | 0.000 | 0.399 | 0.934 | 0.207 | 0.239 | |||
| MSMT (mm) | R | r | 0.073 | 0.003 | 0.113 | 0.013 | 0.264 | -0.064 | |
| P* | 0.646 | 0.987 | 0.477 | 0.934 | 0.091 | 0.689 | |||
| L | r | 0.046 | 0.156 | -0.035 | 0.199 | 0.264 | 0.241 | ||
| P** | 0.770 | 0.322 | 0.824 | 0.207 | 0.091 | 0.125 | |||
| NSBT(mm) | r | -0.019 | 0.138 | -0.065 | 0.186 | -0.064 | 0.241 | ||
| P* | 0.907 | 0.384 | 0.681 | 0.239 | 0.689 | 0.125 | |||
| Age | r | -0.028 | 0.204 | -0.094 | 0.079 | 0.144 | 0.148 | 0.242 | |
| P** | 0.862 | 0.196 | 0.552 | 0.620 | 0.362 | 0.351 | 0.122 | ||
| Gender (Code 1: Male, Code 2: Female) | r | -0.167 | 0.000 | -0.096 | 0.041 | -0.409 | -0.413 | -0.086 | |
| P** | 0.291 | 10.000 | 0.544 | 0.795 | 0.007 | 0.007 | 0.586 | ||
* p value shows the results of Pearson correlation test
** p value shows the results of Spearman’s correlation rho efficient test
ITMT: inferior turbinate mucosal thickness; ITW: inferior turbinate width; MSMT: maxillary sinus mucosal thickness; NSBT: nasal septal body thickness
Discussion
Laryngopharyngeal Reflux (LPR) is a disease caused by inflammation of the upper respiratory-digestive system as a result of reflux of gastroduodenal contents. It causes nonspecific complaints such as sore throat, voice disorders, difficulty in swallowing and chronic cough. It has also been found to be associated with chronic pharyngitis, subglottic stenosis, granuloma, vocal cord nodules, premalignant lesions of the larynx and squamous cell carcinoma [7, 8]. Gastroesophageal reflux disease is seen in 57–80% of patients with clinical signs of LPR [9, 10]. LPR should also be considered in patients who do not have gastroesophageal reflux disease complaints. Although the 24-hour double-probe pH monitoring is recommended as the gold standard method for the diagnosis of LPR, more practical and faster subjective tests are frequently used. In our study, patients diagnosed with LPR according to physical examination and RSI and RFS were included in the study.
PNSCT gives detailed information about nasal and paranasal structures. It helps which surgical technique to be used in pathologies related to paranasal sinuses, septum and turbinates. The major disadvantage of PNSCT is the radiation that the patient will be exposed to. The medial and lateral mucosal thickness and volume of the inferior turbinate can be measured by PNSCT. El-Anwar et al. measured the medial and lateral mucosal thickness of IT and reported that PNSCT measurements are an easy and valuable technique [11]. Similarly, PNSCT has been used in many studies for the measurement of nasal septal body and maxillary sinus mucosal thickness [12, 13]. In our study, ITMT, ITW, MSMT and NSBT were were measured with PNSCT.
The effect of LPR on the size of IT, NSB and maxillary sinus mucosa thickness has not been evaluated in the literature. Various studies have reported that chronic rhinosinusitis is associated with LPR [14, 15]. Yeo et al. reported that LPR symptoms and chronic rhinosinusitis symptoms were associated [14]. In another study, it was reported that there was a significant regression in both LPR and chronic rhinosinusitis complaints in patients given Omeprazole [16]. In our study, bilateral maxillary sinus mucosal thickness values were found to be significantly higher in patients with LPR than in the control group. In males, MSMT values were significantly higher than those in the females. This result was evaluated as a result of the relationship between LPR and chronic rhinosinusitis. Many studies have been conducted between LPR and allergic rhinitis [17, 18]. However, no study has evaluated the relationship between inferior turbinate and LPR. Alharethy et al. showed in their study that LPR increases allergic symptoms and there is a relationship between LPR and allergic rhinitis [17]. Kakaje et al. examined the relationship between LPR, asthma and allergic rhinitis in their study and found a significant relationship between three diseases [18]. In our study, we investigated the relationship of ITMT, which can be a symptom of allergic rhinitis and LPR. The right-ITMT was found to be significantly higher in LPR patients compared to the control group. While the left-ITT was found to be thicker in the LPR group, no significant difference was found compared to the control group. Moreover, ITW values of the LPR group were significantly higher than those in the control group bilaterally. In the LPR group, there were positive correlations between ITMT and ITW values of the right side; and left side separately.We thought that significant results could be obtained in larger series.
The NSB is an erectile structure like the inferior turbinate. The relationship between LPR and NSB has not been investigated before. Hızlı et al. reported that NSB thickness was higher in patients with IT hypertrophy [19]. They also reported that allergic rhinitis causes an increase in NSB thickness [19]. In our study, it was shown that LPR was related to increase NSBT more than that is in the control group, but there was no significant difference between the two groups.
Limitations
The limitations of our study include measuring the structures in one way and not using the 24-hour double-probe pH monitoring in the diagnosis of LPR. Also, studies can be detailed in larger series with different measurement techniques.
Conclusion
In our study, the effects of LPR on ITMT, ITW, MSMT and NSBT were investigated. Right ITMT, bilateral ITW and MSMT values were found to be significantly higher in the LPR group than in the control group. MSMT values were higher in males. The left-ITT and NSBT values were not significantly different between the LPR group and the control group, but both values were higher in the LPR group than in the control group. It was considered that these two values could be found to be significantly higher in larger series. The negative effects of LPR on nasal and paranasal mucosa and structures were demonstrated in this study. LPR related mucosal thickness increase in inferior turbinate and nasal septal body may also cause nasal obstruction.
Acknowledgements
This research did not receive any specifc grant from funding agencies in the public, commercial, or not-for-proft sectors.
Author contribution
BMT: Planning, designing, data collection, literature survey, statistical analysis, interpretation of the results, writing. PZBS: planning, designing, data collection, literature survey, interpretation of the results. ZŞ: planning, designing, literature survey, interpretation of the results. EC: planning, designing, literature survey, interpretation of the results. NBM: planning, designing, literature survey, interpretation of the results, active intellectual support. All authors have contributed signifcantly, and that all authors are in agreement with the manuscript.
Funding
No funds were received for this study.
Data Availability
The data generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. Patient images are stored in the private archive of our faculty and can be shared by the corresponding author upon reasonable request.
Declarations
Ethics approval and consent to participate
This study is retrospective. Ethics committee approval was obtained from Kırıkkale University Non-invasive Researches Ethics Committee (Date: 27.04.2022, Number: 2022.04.21). There is no need to take informed consent, because the data was evaluated retrospectively.
Conflict of interest
The authors declared no potential conflicts of interest concerning the research, authorship and/or publication of this article.
Footnotes
Publisher’s Note
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. Patient images are stored in the private archive of our faculty and can be shared by the corresponding author upon reasonable request.