Changes in Incidental Paranasal Sinus Abnormalities During the COVID-19 Era: A 5-Year MRI-Based Study
Article information
Abstract
Background and Objectives
The coronavirus disease 2019 (COVID-19) pandemic and associated nonpharmaceutical interventions, including mask-wearing and hand hygiene, have led to a global decline in otorhinolaryngologic conditions, with the monthly incidence of chronic rhinosinusitis decreasing from 39.49 to 14.56 per 100,000 people. This study compared the prevalence and severity of paranasal sinus abnormalities observed on magnetic resonance imaging (MRI) before and during the COVID-19 pandemic.
Methods
This retrospective study analyzed brain MRI scans from 3,762 individuals (1,881 men and 1,881 women; mean age, 56.2±9.8 years) performed at a single health-screening center in Seoul, South Korea, between January 2018 and December 2022. The study period was divided into pre-COVID-19 and COVID-19 phases, with March 2020 as the cutoff. A total of 428 scans demonstrating incidental paranasal sinus abnormalities, including mucosal thickening, retention cysts or polyps, fluid collection, and fungal balls, were evaluated using the Lund-Mackay (LM) scoring system.
Results
The overall prevalence of incidental paranasal sinus abnormalities was 11.4% (428/3,762), with a significant decline from the pre-COVID-19 to the COVID-19 period (16.1% vs. 8.6%, p<0.001). However, the mean LM score among participants with abnormalities was significantly higher during the COVID-19 period than in the pre-COVID-19 period (3.64±3.22 vs. 3.01±2.58, p=0.026). The proportion of nasal polyps was also greater during the COVID-19 period than in the pre-COVID-19 period (10.8% vs. 5.8%, p=0.028).
Conclusion
The prevalence of incidental paranasal sinus abnormalities on MRI decreased during the COVID-19 period compared to the pre-COVID-19 period, whereas the severity, as reflected by the LM score, increased.
INTRODUCTION
The coronavirus disease 2019 (COVID-19) pandemic, caused by severe acute respiratory syndrome coronavirus 2 (SARSCoV-2), had profound effects on multiple aspects of daily life worldwide [1]. To prevent its spread, nationwide nonpharmaceutical interventions (NPIs) were implemented, including personal protective measures to improve health-seeking behaviors and hygiene practices [2]. Recent studies have reported sharp declines in the monthly prevalence of acute sinusitis, acute tonsillitis, and otitis media during the COVID-19 period, from 1.08% to 0.49%, 1.32% to 0.56%, and 0.69% to 0.30%, respectively [3]. Similarly, the monthly age- and sex-specific incidence rate of chronic rhinosinusitis (CRS) decreased from 39.49 to 14.56 per 100,000 people [4]. To date, however, no study has specifically examined changes in the prevalence or severity of paranasal sinus abnormalities associated with the COVID-19 pandemic.
Magnetic resonance imaging (MRI) has substantially advanced diagnostic capabilities by providing detailed, noninvasive visualization of internal structures [5]. Therefore, MRI screening is now widely used during health checkups in asymptomatic individuals. Brain MRI encompasses the paranasal sinuses, enabling detection of incidental abnormalities. Several prior studies have evaluated paranasal sinus abnormalities incidentally detected on brain MRI [6-8].
This study aimed to investigate differences in the prevalence and severity of paranasal sinus abnormalities detected on brain MRI in individuals undergoing routine health checkups before and during the COVID-19 pandemic.
METHODS
This retrospective study was approved by the Institutional Review Board of Kangbuk Samsung Hospital (IRB_No. KBSMC 2023-06-034). Due to the retrospective nature of the study, the requirement for written informed consent was waived. All study procedures were conducted in accordance with the relevant guidelines and regulations.
Study population
Between January 2018 and December 2022, a total of 147,235 individuals visited our health screening center in Seoul, South Korea. Of these, 3,762 individuals (1,881 men and 1,881 women; mean age, 56.2±9.8 years; range, 13–87 years) underwent brain MRI scans, and all were included in this study. For analysis, the period from January 2018 to February 2020 was defined as pre-COVID-19, and March 2020 to December 2022 as the COVID-19 period, corresponding to the detection of the first confirmed COVID-19 case in Korea on January 20, 2020, and the initiation of nationwide prevention and control measures in March 2020 [3]. Individuals with a prior diagnosis of rhinosinusitis (n=2) and those with a history of sinus surgery (n=29) were excluded, based on a review of medical records. In addition, 104 MRI scans were excluded as follow-up examinations from individuals who underwent multiple scans during the study period (Fig. 1). During the COVID-19 period, individuals presenting with respiratory symptoms such as fever (≥37.5°C), chills, myalgia, cough, ageusia, anosmia, sore throat, or dyspnea were not permitted to undergo health screenings and were therefore excluded from this study.
MRI acquisition and image analysis
Brain MRI was performed using a 1.5 T unit equipped with a 16-channel head coil (SIGNA HDxt 1.5T; GE Healthcare). The standard brain MRI protocol included: 1) axial images extending from the vertex of the skull to the hard palate, 2) coronal images from the facial region to the temporomandibular joint, and 3) sagittal images covering the entire head from the vertex to the chin.
Two rhinologists and one radiologist independently reviewed, and then reached consensus on, axial and coronal T1- and T2-weighted images (WI). Among the scans reviewed, 3,334 participants showed normal sinus findings. Detailed scoring was conducted for the remaining 428 cases to assess the severity of abnormalities. The Lund-Mackay (LM) scoring system was applied to evaluate the opacification of the bilateral frontal, anterior ethmoid, posterior ethmoid, maxillary, and sphenoid sinuses, as well as the ostiomeatal units, assigning scores from 0 to 2, with a maximum total score of 24 [9]. The basal lamella of the middle turbinate was used to separate the anterior from the posterior ethmoid sinuses [10], with landmarks including the ethmoid bulla and both the vertical and horizontal portions of the middle turbinate. Mucosal thickening >3 mm in the frontal, ethmoid, maxillary, or sphenoid sinuses was considered positive [8]. A retention cyst or polyp was defined as a high-signal lesion with a bulging contour within the sinus on T2-WI. Fluid collection was defined as the presence of an air-fluid level within the sinus. A fungal ball was characterized by low signal intensity (SI) on T2-WI and high SI on T1-WI [11].
Additional nasal findings—including septal deviation, inferior turbinate (IT) hypertrophy, concha bullosa, and nasal polyps—were also evaluated. The degree of septal deviation was quantified by measuring the angle between the point of maximal deviation on the coronal view and the midline connecting the crista galli to the nasal floor. An angle ≥9° was considered indicative of prominent septal deviation [12-15]. Although computed tomography (CT)-based criteria for evaluating IT hypertrophy are limited, prior studies have reported mean IT widths of 9.3–10.97 mm in affected patients [16,17]. To comprehensively assess hypertrophy involving both the mucosa and bone, the total IT width was measured, with hypertrophy defined as a width ≥10 mm on either side. On T2-WI, convex lesions with high SI located in the middle or superior meatus were regarded as nasal polyps.
Statistical analysis
Statistical analyses were conducted using SPSS for Windows (version 24.0, IBM Corp.), and a p-value <0.05 was regarded as statistically significant. Age, sex, and prevalence of abnormal sinus findings were compared between the pre-COVID-19 and COVID-19 groups in the full cohort of 3,762 participants using t-tests or chi-square tests. Further analyses were conducted in the 428 individuals with abnormal sinus findings, comparing age, sex, the distribution of affected sinuses (frontal, ethmoid, maxillary, and sphenoid), MRI findings (mucosal thickening, retention cyst or polyp, fluid collection, and fungal ball), nasal findings (septal deviation, IT hypertrophy, concha bullosa, and nasal polyp), and LM scores using the t-test or chi-square test. Analysis of covariance was applied to adjust LM scores for age. In addition, the t-test was used to analyze differences in LM scores based on the presence or absence of abnormal MRI findings in the paranasal sinuses and nasal cavity.
RESULTS
Table 1 summarizes the baseline characteristics of the study participants. Of the 3,762 patients who underwent brain MRI, 1,395 (37.1%; 695 men and 700 women) were scanned during the pre-COVID-19 period, and 2,367 (62.9%; 1,186 men and 1,181 women) during the COVID-19 period. No significant difference was found between the two groups in terms of sex distribution (p=0.866). The mean age of all participants was 56.2±9.8 years. Patients in the pre-COVID-19 group (mean, 55.7±9.7 years; range, 13–87 years) were significantly younger than those in the COVID-19 group (mean, 56.6±9.9 years; range, 15–82 years, p=0.007). The overall prevalence of paranasal sinus abnormalities on MRI was 11.4% (428/3,762), with a significantly higher prevalence in the pre-COVID-19 period (16.1% [224/1,395]) compared with the COVID-19 period (8.6% [204/2,367]; p<0.001). By year, the prevalence of abnormal sinus findings was 20.1% in 2018, 15.1% in 2019, 5.1% in 2020, 7.8% in 2021, and 9.8% in 2022.
Table 2 presents details of the 428 individuals with abnormal sinus findings. Across the entire group, men were significantly more affected than women (68.5% [293/428] vs. 31.5% [135/428], p<0.001). This sex difference was consistent in both the pre-COVID-19 (67.4% [151/224] vs. 32.6% [73/224], p<0.001) and COVID-19 (69.6% [142/204] vs. 30.4% [62/204], p<0.001) periods. However, no significant difference in sex distribution was observed between the two time periods (p=0.625). Among sinus abnormalities detected on MRI, the maxillary sinus was most commonly affected (404 patients, 94.4%), followed by the ethmoid sinus (210 patients, 49.1%), frontal sinus (66 patients, 15.4%), and sphenoid sinus (59 patients, 13.8%). The distribution of affected sinuses did not significantly differ between the pre-COVID-19 and COVID-19 periods. Regarding types of abnormalities (Fig. 2), mucosal thickening was the most frequent finding (297 cases, 69.4%), followed by retention cysts or polyps (252 cases, 58.9%), fluid collection (64 cases, 15.0%), and fungal balls (35 cases, 8.2%). These frequencies did not significantly differ between the two periods. In the nasal cavity (Fig. 3), IT hypertrophy was the most common finding (418 patients, 97.7%), followed by deviated septum (343 patients, 80.1%), concha bullosa (72 patients, 16.8%), and nasal polyps (37 patients, 8.6%). The prevalence of nasal polyps increased significantly during the COVID-19 period compared with the pre-COVID-19 period (11.8% vs. 5.8%, p=0.028), whereas other nasal findings showed no significant changes.
Characteristics of study populations with abnormal MRI findings in the pre-COVID-19 and COVID-19 periods
Abnormal paranasal sinus findings on brain MRI. A: Mucosal thickening. On coronal T2-weighted imaging (WI), mucosal thickening greater than 3 mm (arrow) is observed in the left maxillary sinus. B: Retention cyst. On coronal T2-WI, a retention cyst (bold arrow) is observed in the left maxillary sinus. C: Fluid collection. On axial T2-WI, an air-fluid level (arrowheads) consistent with fluid collection is observed in both maxillary sinuses. D and E: Fungal ball. On axial T2-WI (D), a fungal ball (empty arrow) with low signal intensity (SI) is visible in the left maxillary sinus. In the corresponding axial T1-WI (E), the fungal ball (empty arrowhead) demonstrates iso- to high SI.
Abnormal findings of the nasal cavity on brain MRI. A: On coronal T2-weighted imaging (WI), bilateral concha bullosa (arrows), rightward deviation of the nasal septum (bold arrow), and bilateral inferior turbinate hypertrophy (arrowheads) are observed. B: On coronal T2-WI, a right nasal polyp (empty arrow) is observed.
The overall mean LM score among participants with sinus abnormalities was 3.31±2.92. During the COVID-19 period, the LM score was significantly higher than in the pre-COVID-19 period (3.64±3.22 vs. 3.01±2.58, p=0.026). In the pre-COVID-19 period, LM scores ranged from 1 to 20: 58.0% of participants scored 1–2, 24.2% scored 3–4, 8.9% scored 5–6, and 8.7% scored ≥7 (Fig. 4). In the COVID-19 period, LM scores ranged from 1 to 19, with lower proportions scoring 1–2 (52.5%) and 3–4 (17.2%) and higher proportions scoring 5–6 (16.7%) and ≥7 (13.8%) compared with the pre-COVID-19 period. After adjusting for age, the least squares mean LM score was significantly higher during the COVID-19 period (3.64; standard error, 0.20) compared with the pre-COVID-19 period (3.00; standard error, 0.19) (p=0.025).
Analysis of MRI findings of paranasal sinus abnormalities (Table 3) showed that the mean LM score was significantly higher in patients with mucosal thickening (4.07±3.18 vs. 1.57±0.68, p<0.001), fluid collection (4.22±3.99 vs. 3.15±2.66, p=0.043), and fungal balls (4.31±3.34 vs. 3.22±2.86, p=0.033) compared with those without these findings. In contrast, the presence of retention cysts or polyps was not associated with a significant difference in LM scores (p=0.482). Among nasal cavity abnormalities (Table 3), the mean LM score was significantly higher in patients with nasal polyps (8.46±4.83 vs. 2.82±2.10, p<0.001). Other nasal findings were not associated with significant differences in LM scores.
DISCUSSION
In this study, incidental sinus findings detected on brain MRI scans were analyzed by comparing data from large-scale health examinations conducted before and during the COVID-19 pandemic. The prevalence of incidental sinus findings was 16.1% in the pre-COVID-19 period, which decreased significantly to 8.6% during the COVID-19 period. Annual prevalence data showed a sharp decline beginning in 2020 with the onset of the pandemic. However, the mean LM score of participants with sinus abnormalities was significantly higher during the COVID-19 period compared with the pre-COVID-19 period. The age-adjusted LM score also remained significantly higher during the COVID-19 period.
As COVID-19 spread globally, South Korea implemented nationwide public health measures, including NPIs, beginning in March 2020 [3]. Mask-wearing became mandatory both indoors and outdoors, frequent handwashing was widely encouraged, and appropriate physical distancing in public spaces was recommended. Large gatherings in private settings were also restricted. Individuals presenting with fever or respiratory symptoms were prohibited from attending school or work and were instructed to self-quarantine at home or in designated facilities [2]. Reportedly, the prevalence of several infectious otolaryngologic diseases, such as acute tonsillitis, acute sinusitis, and otitis media, declined following the introduction of these measures [3]. This phenomenon has been attributed not only to NPIs but also to reduced visits to medical institutions by patients with mild symptoms, largely due to concerns about contracting COVID-19 [18].
In our study, the frequency of incidental sinus findings also decreased during the pandemic, likely as a result of NPIs. An air-fluid level, a radiologic finding associated with acute rhinosinusitis, has been reported in 25%–50% of patients with acute sinusitis [19]. In the present study, this finding was defined as fluid collection and was observed in 15.0% of individuals with sinus abnormalities on MRI, with no significant difference in proportion between the pre-COVID-19 and COVID-19 periods. During the COVID-19 period, although the prevalence of sinus abnormalities among all participants decreased, the proportion of fluid collection among individuals with abnormalities remained unchanged. Therefore, the absolute prevalence of fluid collection in the total population can also be considered to have decreased. These findings suggest that NPIs, by preventing viral and bacterial upper respiratory infections, played an important role in reducing the prevalence of sinus abnormalities during the pandemic. At the same time, the similar proportions of most sinus abnormalities before and during the COVID-19 period indicate that additional factors beyond NPIs, such as restricted access to healthcare services and health screenings, may have also influenced these results. Notably, the proportion of nasal polyps among incidental MRI findings was significantly higher after the pandemic. Because patients with nasal polyps exhibited significantly higher LM scores than those without, the increased proportion of polyps may partly explain the overall rise in LM scores during the COVID-19 period. One study reported that patients with CRS without nasal polyps had a higher risk of contracting COVID-19 (odds ratio, 1.24), whereas patients with CRS and nasal polyps showed a neutral association [20]. This observation may suggest that patients with nasal polyps had relatively better access to health screenings during the pandemic.
In the adult population, the prevalence of CRS without nasal polyps has been reported as 5.8%, CRS with nasal polyps as 2.6%, and overall CRS as 8.4% [21]. Although these figures are approximately half the prevalence of sinus abnormalities observed in the pre-COVID-19 period in our study (16.1%), it should be noted that our findings also included radiologic abnormalities not necessarily related to CRS, such as retention cysts. Considering the reported decline in CRS prevalence during the COVID-19 pandemic, the trend observed in our study appears consistent with previous reports [4,22]. Among participants with sinus abnormalities, retention cysts or polyps were identified in 58.9% and nasal polyps in 8.6%. Notably, 108 individuals (25.2%) had only a retention cyst without any other abnormality, a distribution resembling that of CRS with nasal polyps in the general population. A previous study reported that between 2005 and 2010, the prevalence of fungal balls confirmed by calcification on CT in CRS patients was 1.9%, with an increasing trend over time [23]. In our study, fungal balls were detected in 8.2% of individuals with sinus abnormalities, a rate higher than previously reported. One study found that 89.1% of fungal balls exhibited hyperintense signal portions on T1-WI MRI, whereas calcification was identified on CT in only 89.8% of cases [24]. These findings suggest that MRI may play an important role in detecting fungal balls. Furthermore, because fungal balls can remain asymptomatic and be discovered incidentally, such cases may have contributed to the relatively high prevalence observed in our study [25].
MRI can also be advantageous for differentiating sinus lesions. Edema or inflammatory lesions with high water content typically appear as areas of high SI on T2-WI [26]. Thus, even when MRI is performed for indications unrelated to sinus disease, such as brain imaging, it can provide valuable information about the nasal cavity and paranasal sinuses [19]. Previous studies have investigated incidental sinus findings on MRI performed for other purposes, with reported prevalence rates ranging widely from 11.6% to 66.2% (Table 4) [6-8,27-30]. In our study, the overall prevalence was 11.4%, while the pre-COVID-19 prevalence was 16.1%. This value is somewhat lower than that reported in many earlier studies; however, because our analysis was based on large-scale health screening data, it may more accurately represent the prevalence of sinus abnormalities in the general population. In contrast, Hansen et al. [7] reported a prevalence of 66.2% of incidental sinus findings on MRI performed for public health survey purposes. Their study, however, included very minor lesions as small as 1 mm, which necessitates cautious interpretation.
While mucosal thickening may indicate acute or chronic sinusitis [31], minimal thickening is often a normal finding associated with the nasal cycle rather than a pathological change [26]. Other studies that applied a threshold of ≥3 mm for mucosal thickening reported prevalence rates of 50%–84.6% for mucosal thickening, 33.3%–42.4% for retention cysts or polyps, and 2.3%–6.8% for fluid collection [8,28,30]. In this study, we also defined mucosal thickening as >3 mm, and the prevalence of retention cysts or polyps and fluid collection was somewhat higher than in those earlier reports. Given that brain MRI typically uses wider slice intervals, certain abnormalities may have been missed. Therefore, reviewing not only coronal but also axial and sagittal views can improve diagnostic accuracy. Additionally, it is essential to examine both T1- and T2-WI when assessing the sinuses, as fungal balls may mimic air on T2-WI alone, leading to underestimation. To the best of our knowledge, fungal sinusitis has rarely been reported in English-language literature, with only one study documenting an incidence of 2.3% [30]. In comparison, our study observed a prevalence of 8.2% for fungal balls, highlighting the need for further evaluation of these findings in future research.
The LM score is a simple and widely used method in sinus research [9]. However, it does not always accurately reflect disease severity, as partial opacification (scored as one point) covers a broad range of findings. Moreover, LM scores in normal populations have been reported to vary from 2.2 to 4.26 [32,33], and some studies have considered scores of 4 or higher as abnormal [6,34]. In our study, 10.1% (13/129) of participants with an LM score of 2 had total opacification (2 points). Among those with an LM score of 3, 20.0% (13/65) showed total opacification, and among those with an LM score of 4, 29.2% (7/24) demonstrated total opacification. These findings indicate that caution is required when interpreting low LM scores, as it would be inappropriate to uniformly regard them as normal or dismiss them as clinically insignificant. In this study, participants with mucosal thickening had significantly higher LM scores than those without mucosal thickening. Among individuals without mucosal thickening, retention cysts were the most common finding (90.0%), followed by fluid collections (15.0%) and fungal balls (2.3%). Furthermore, 76.3% of these lesions were confined to the maxillary sinus. Additionally, the higher LM scores observed in cases with fluid collection and fungal balls suggest that these abnormalities are indicative of more severe pathological conditions. CRS with nasal polyps is known to present with more severe radiological findings than CRS without polyps [35], which is consistent with our results.
This study has several limitations. First, it was a retrospective study conducted in participants who voluntarily underwent health checkups at a single healthcare center. Most participants were employees of companies, members of local government organizations, or their family members, rather than individuals enrolled in the national cancer screening program. Thus, the findings may not be fully representative of the general population, and selection bias is inevitable. Nevertheless, the study mitigated some of these issues by including a large dataset of 3,762 individuals over 5 years. Second, participants were included based on undergoing brain MRI for screening, without data on rhinosinusitis-related symptoms, limiting the ability to correlate clinical symptoms with imaging findings. In addition, nasal polyps were evaluated solely by MRI without endoscopic confirmation, which restricts the accuracy of reflecting the true prevalence, and results should therefore be interpreted with caution. Third, the observed decrease in the prevalence of incidental sinus findings during the COVID-19 period cannot be definitively attributed to the pandemic. Further research is needed to clarify whether this trend persists after the pandemic and to better understand its underlying mechanisms. Fourth, brain MRI may lack complete coronal views or fail to capture the inferior regions of the maxillary sinuses and nasal cavity, which can complicate evaluation of sinonasal structures. Moreover, slice thickness in brain MRI is often too large to reliably assess ostiomeatal unit (OMU) patency. Despite these limitations, the MRIs performed at our institution included the full nasal cavity and paranasal sinuses in the coronal plane, permitting adequate evaluation. Although slice thickness was relatively large, it did not substantially hinder the assessment of OMU patency.
In conclusion, the prevalence of incidental sinus findings detected on MRI decreased during the COVID-19 period compared with the pre-COVID-19 period, while the LM score increased. These results are likely influenced by multiple factors, including NPIs and reduced access to healthcare. Further prospective studies are warranted to clarify the mechanisms underlying these observations.
Notes
Availability of Data and Material
The datasets generated and analyzed during the current study are not publicly available due to institutional restrictions, but are available from the corresponding author upon reasonable request.
Conflicts of Interest
The authors have no potential conflicts of interest to disclose.
Author Contributions
Conceptualization: Inyoung Youn, Kyung Chul Lee. Data curation: Seongjin Yun, Soojin Jung, Hayoung Byun, Hyebin Lee, Inyoung Youn, Kyung Chul Lee. Formal analysis: Jae-Seon Park, Suhyeon Moon, Inyoung Youn. Investigation: Jae-Seon Park, Jae Wook Kim, Hyebin Lee, Inyoung Youn, Kyung Chul Lee. Methodology: Seongjin Yun, Suhyeon Moon, So Young Han. Software: Jae-Seon Park, Seongjin Yun, Suhyeon Moon. Writing— original draft: Jae-Seon Park, Seongjin Yun, Inyoung Youn. Writing— review & editing: Suhyeon Moon, Seongjin Yun, Jae Wook Kim, Soojin Jung, Hayoung Byun, Kyung Chul Lee.
Funding Statement
None
Acknowledgments
None
