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ORIGINAL ARTICLE
Year : 2021  |  Volume : 24  |  Issue : 8  |  Page : 1200-1205

Comparison of Airway Measurements in Rheumatoid Arthritis and Non-rheumatoid Patients using Lateral Cephalometric Radiographs


1 Department of Oral Diagnostic Sciences, King Abdulaziz University, Jeddah, Saudi Arabia
2 Department of Oral and Maxillofacial Surgery, King Abdulaziz University, Jeddah, Saudi Arabia
3 Department of Dental Public Health, King Abdulaziz University, Jeddah, Saudi Arabia
4 Sleep Medicine and Research Group, Sleep Medicine and Research Center, King Abdulaziz University, Jeddah, Saudi Arabia
5 Department of Medicine, Faculty of Medicine, University of Jeddah, Jeddah, Saudi Arabia
6 Department of Medicine, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia
7 Department of Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia

Date of Submission06-Jun-2020
Date of Acceptance30-Nov-2020
Date of Web Publication14-Aug-2021

Correspondence Address:
Dr. F F Badr
Department of Oral Diagnostic Sciences, Faculty of Dentistry, King Abdulaziz University. P. O. Box: 80209, Jeddah 21589
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_336_20

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   Abstract 


Objective: The aim of this study was to investigate the potential relationship between the volumetric area of the upper airway and rheumatoid arthritis (RA) by comparing upper airway measurements between patients with and without RA. Methods: This case-control study compared upper airway measurements between patients with and without RA using lateral cephalometric radiographs. Two distinct measurements were made: the area of the upper airway, which is defined as “the area extending from the point of the retro-palatal region to the base of the epiglottis,” and the distance of the upper airway, which is defined as “the distance between the anterior border of the third cervical vertebra (C3) and the anterior border of the soft tissue of the neck“. A single examiner performed all measurements, and the intra-examiner reliability was assessed. Results: Sixty-one RA patients and 95 non-RA patients were included in the case and control groups, respectively. RA patients were significantly older in age and with higher BMI values. Patients with or without RA had Angle Class II as the most prevalent orthodontic classification. The upper airway was slightly narrower in RA patients, resulting in a smaller area, and the length of the upper airway was significantly longer in RA patients. Conclusion: Patients with RA have narrower upper airways as measured on lateral cephalometric radiographs. This may partially explain the high prevalence of obstructive sleep apnea among patients with RA. Focusing on airways measurements when cephalometric radiographs are taken for patients with RA could give some idea about which patient is likely to have OSA.

Keywords: Cephalometry, dental imaging, diagnostic imaging, rheumatoid arthritis, sleep apnea, upper airway


How to cite this article:
Badr F F, Jadu F M, Nasir A M, Jan A M, Wali S, Mustafa M, Bawazin Y, Meisha D. Comparison of Airway Measurements in Rheumatoid Arthritis and Non-rheumatoid Patients using Lateral Cephalometric Radiographs. Niger J Clin Pract 2021;24:1200-5

How to cite this URL:
Badr F F, Jadu F M, Nasir A M, Jan A M, Wali S, Mustafa M, Bawazin Y, Meisha D. Comparison of Airway Measurements in Rheumatoid Arthritis and Non-rheumatoid Patients using Lateral Cephalometric Radiographs. Niger J Clin Pract [serial online] 2021 [cited 2022 Jan 22];24:1200-5. Available from: https://www.njcponline.com/text.asp?2021/24/8/1200/323851




   Introduction Top


Rheumatoid arthritis (RA) is one of the most commonly encountered chronic disorders in Saudi Arabia.[1],[2] It is divided to seropositive RA and seronegative groups. The seropositive group is defined as a patient who has a positive rheumatoid factor (RF) or anti-cyclic citrullinated peptide (anti-CCP), or both. It indicates a more aggressive disease and poor prognostic outcome.[3] While the seronegative group contains patients who have clinical features of RA with negative RA specific antibodies (RF and anti-CCP).[3] The variability of the disease presentation requires improvements in our current level of understanding, which will translate to an improved standard of care for our patients. RA patients are at risk of airway obstruction, particularly when the temporomandibular joints (TMJs) are involved.[4] Involvement of the TMJs can also lead to obstructive sleep apnea (OSA) as a result of the reduced ramus height and the downward and backward rotation of the mandible.[5] Previous studies have also demonstrated that patients with OSA have larger neck circumferences and thicker soft tissues in the neck.[6]

The cross-sectional area of the airway in patients with RA were evaluated in the past using CT imaging.[7],[8] However, the effect of this condition on the volumetric area of the upper airway has not been evaluated before using conventional two-dimensional (2D) radiography. We are of the opinion that 2D lateral cephalometric radiographs rather than CT scans can be used to measure the upper airway area as well as the neck soft-tissue thickness in patient with RA, and therefore give some idea as to which patient is likely to have OSA. This imaging modality is not only accessible and economical, but also reliable and reproducible for this purpose.[9],[10],[11],[12] The effective dose of a lateral cephalometric image is 2-6 micro Sieverts, which is equivalent to 0.3-0.7 days of background exposure.[13],[14],[15] The upper airway area, as depicted in 2D radiographs, has been found to have a positive association with the cone beam CT (CBCT) airway volume, yet 2D radiographs offer a significantly lower radiation dose alternative.[10],[16] The effects of narrowing and obstruction of this crucial area is important in the field of craniofacial orthodontics.[17] The aim of this study was to investigate the potential relationship between the upper airway area and neck soft-tissue thickness using simple measurements from cephalometric radiographs in patients with and without RA. The hypothesis of this study was that RA patients would have narrower upper airway spaces and thicker neck soft tissues compared to non-RA patients, which may explain the high prevalence of OSA among these patients.


   Methods Top


The study protocol was approved by the King Abdulaziz University Faculty of Dentistry (KAUFD) research ethics committee (no. 111-06-19) and conforms to the principles of the Helsinki declaration. The study uses a case-control design in which rheumatoid arthritis patients were compared to medically healthy orthodontic patients. Rheumatoid arthritis patients that needed an airway assessment were recruited in collaboration with King Abdulaziz University Hospital (KAUH), and these constituted the case group (Group 1). The control group (Group 2) was recruited concurrently from medically healthy patients seeking orthodontic care at KAUFD. Written informed consent was obtained from each patient before they were given appointments for the acquisition of lateral cephalometric radiographs at the same center. No additional imaging was done for the control group as they received lateral cephalometric radiographs for orthodontic treatment purposes as part of the routine pretreatment orthodontic records. Orthodontic patients with systemic diseases or sleep-related breathing disorders (e.g., OSA) were excluded. Inclusion criteria included availability of diagnostic quality lateral cephalometric radiographs of patients over the age of 18 years. Demographic characteristics along with height and weight measurements were collected, with which body mass index values were calculated.

Upper airway measurements were obtained using the millimeter ruler and the lateral cephalometric radiographs. The picture elements (pixels) were converted to square millimeters. The polygon tool was used to obtain the airway area. Two distinct measurements were made: the first was the upper airway “area” defined as “the area extending from the point of the retro-palatal region to the base of the epiglottis.” The second measurement was of the upper airway “distance” defined as “the distance between the anterior border of the third cervical vertebra (C3) and the anterior border of the soft tissue of the neck” [Figure 1]. This is a simple measurement for neck soft-tissue thickness. All airway measurements were performed by a single examiner under the same conditions using Image J® software (National Institute of Health image, public domain). To assess the intra-examiner reliability, sixteen cases were re-measured, ten days apart, by the same examiner.
Figure 1: Lateral cephalometric radiographs demonstrating the upper airway “area” measurement (a) and the upper airway “distance” (b) measurement

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Statistical analyses were performed using the Statistical Package for Social Sciences (IBM®SPSS® Statistics) Version 24.0 software. Normality of airway measurements was assessed using the Shapiro–Wilk test. Descriptive statistics were calculated. The Mann-Whitney test was used to assess if there are any differences between patients with and without rheumatoid arthritis with respect to the airway measurements. Multiple linear regression models were performed to predict airway measurements, while controlling for possible confounders, such as age, gender, BMI, and orthodontic classification. The level of significance was set a priori at 0.05. The intra-class correlation coefficient (ICC) was used to assess intra-examiner reliability in the airway measurements, as it is the most appropriate statistical test to assess reliability for single observations of a continuous measure.[18],[19]


   Results Top


The reliability evaluation showed excellent intra-examiner reliability in upper airway measurements (i.e., the ICC ranged from 0.94 to 0.99). Of the 175 patients considered for inclusion in this study, 156 were eligible [Figure 2]- flowchart of the study sample]. The case group (group 1) included 61 rheumatoid arthritis patients, and the control group (group 2) comprised 95 medically healthy patients seeking orthodontic care at KAUFD. The upper airway distance and area measurements were not normally distributed, as assessed by the Shapiro–Wilk's test (p < 0.0001). A comparison of demographic characteristics between patients with and without RA is summarized in [Table 1]. RA patients were significantly older and had higher BMI values. The majority of the RA cases were females, whereas approximately half of the control group was females. Patients with or without RA had Angle Class II as the most prevalent orthodontic classification, followed by Class I and then Class III. The upper airway was slightly narrower in RA patients compared to non-rheumatoid patients, resulting in smaller areas (means of 479.7 mm2 versus 516.7 mm2 respectively). The upper airway distance was significantly longer in RA patients compared to non-RA patients [Figure 3].
Figure 2: Flowchart of the study sample

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Figure 3: Comparison of upper airway area and distance between patients with and without rheumatoid arthritis. *P < 0.0001

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Table 1: Characteristics of patients with (cases) and without (controls) rheumatoid arthritis (n=155)

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A multiple linear regression model was performed to predict upper airway area and distance while controlling for possible confounders, such as gender, age, BMI, and orthodontic classification. The multiple regression model predicting the area of the upper airway was statistically significant (R2 = 14.3%, P value = 0.02) [Table 2]. RA patients had smaller upper airway areas compared to non-rheumatoid patients (by 57 mm2) while controlling for gender, age, and BMI. Females had significantly smaller upper airway areas (by 129 mm2) compared to males. An increase in age of 1 year was associated with an increase in upper airway area of 1.3 mm2, whereas, an increase in BMI of one unit was associated with a decrease in upper airway area by 0.16 mm2. Regarding the upper airway distance, the multiple regression model was statistically significant and exhibited a better prediction metric than the same model when used for upper airway area (R2 = 62.4%, P = 0.0001) [Table 3]. RA patients had longer upper airway distances compared to non-RA patients (by 80 mm) while controlling for gender, age, and BMI. An increase of 1 year of age is associated with an increase in the upper airway distance by 2.1 mm, whereas an increase of 1 unit of BMI is associated with an increase in the upper airway distance by 3.7 mm.
Table 2: Multiple linear regression model predicting upper airway area

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Table 3: Multiple linear regression model predicting upper airway distance

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   Discussion Top


In the current study, the upper airway was slightly narrower in RA patients, compared with the control, resulting in a smaller area, but this did not reach statistical significance. However, the distance of the upper airway was significantly longer in RA patients. The intra-examiner reliability was excellent (ICC: 0.94-0.99) for the airway measurements. This is in agreement with Ghoneima and Kula who reported high intra-examiner reliability for airway volume measurements (r > 0.90).[20]

To the best of our knowledge, no published studies exist in recent English literature regarding airway measurements in RA patients using simple cephalometry. In contrast, several publications examined airway measurements using advanced imaging techniques such as magnetic resonance imaging (MRI), multidetector CT (MDCT), and CBCT.[21],[22] In the current study, upper airway areas were slightly smaller in RA patients. Burkdull et al. also found an inverse correlation between the retro-lingual airway and the severity of OSA.[23] In our study, the upper airway distance was significantly longer in RA patients. Similarly, MRI studies have revealed that patients with OSA also have thicker soft tissues.[24],[25],[26]

RA patients were significantly older in age and had higher BMI values. These results are a simple reflection of our study populations. RA is an acquired chronic inflammatory condition that usually manifests in older individuals,[27],[28],[29] whereas our control population was relatively younger, since they were seeking orthodontic treatment. Even though we attempted to control for age by choosing patients older than 18 years of age in the control group, there was still a significant difference between the two groups of patients at baseline. Multiple regression models were performed to account for that and to control for possible confounders.

Studies have demonstrated that the prevalence of OSA is higher among patients with RA. This has been attributed to anatomical abnormalities as a consequence of RA, such as micrognathia. The findings in the current study also add another element that may contribute to the high prevalence of OSA among RA patients.

BMI results were also significantly higher for the RA patients. These results are consistent with Albrecht et al.[30] They studied early and established cases of RA and compared their BMI to find that all RA patients had a higher prevalence of obesity than the general population.[30] A meta-analysis conducted by Feng et al. in 2016 concluded that obesity was a risk factor for RA.[31] They also concluded that the association between RA and BMI was greater for females.[31] Indeed, the majority of RA cases in the current study were females. Other studies found that females are not only more at risk to develop RA but are also associated with higher disease activity scores and worse radiographic joint destruction than males.[32],[33] The reason for this female propensity is still unclear, but genetic and hormonal influences are suspected.[34] Another possible explanation could be attributed to the fact that health care-seeking behavior differ by gender.[35] Females tend to seek heath care more than males do and this could be a factor in our study since the majority of our sample were females.

Patients with or without RA had Class II as the most prevalent orthodontic classification. Numerous studies evaluating the orthodontic classification of patients with juvenile RA claim Class II to be the most prevalent.[36],[37],[38] However, the literature is bereft of data regarding the orthodontic classification in adult patients with RA. With regards to the non-RA control patients, distribution of malocclusion classification is slightly different than that of Aldrees, who in 2012 studied the patterns of skeletal and dental malocclusion in Saudi orthodontic patients and found Angle Class II to be the second most common classification after Class I.[39] This could be attributed to the fact that although class I malocclusion is the most prevalent malocclusion classification, however, orthodontic patients with mild class I malocclusion usually do not require acquisition of cephalometric radiograph, which is one of our inclusion criteria. The study has several limitations including the inherent limitation of the case-control study design. Another limitation is using only cephalometric radiographs (2D) to evaluate the airway. A third limitation is the differences in age, gender, orthodontics classification between rheumatoid and non-rheumatoid arthritis patients. However, this limitation was overcome by performing multiple linear regression models to control for the possible confounders. One of the study strength points is performing airway measurements by a single calibrated examiner with high intra- examiner reliability (ICC > 0.94).


   Conclusion Top


Patients with RA have narrower upper airways as measured on lateral cephalometric radiographs. This may partially explain the high prevalence of OSA among patients with RA. The findings of this study suggest paying attention to airways measurements when cephalometric radiographs are taken for patients with RA. This could give some idea about which patient is likely to have OSA.

Financial support and sponsorship

This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under grant no. RG-01-140-38. The authors, therefore, acknowledge with thanks DSR for technical and financial support.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

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