Abstract
Objectives
We aimed to investigate the prevalence and age-related changes in vestibular function within the general population using survey data from the Korean National Health and Nutrition Examination Survey (KNHANES) and examine the potential factors influencing it.
Methods
We analyzed retrospective data from 1270 participants from the 2021 KNHANES who completed both the video head impulse test and audiometric evaluations. Participants with vestibulo-ocular reflex (VOR) gains <0.8 and >1.2 were excluded to minimize the impact of possible testing errors and prior impaired vestibular function. We assessed the prevalence and age-related changes in vestibular function and analyzed potential influencing factors using logistic regression analysis.
Results
The VOR gain decreased with age; however, statistical significance was not achieved (coefficient −0.0003, p = 0.281). The presence of corrective saccades significantly increased with age (p < 0.001), with those in their 70s being 3.98 times more likely to exhibit corrective saccades than those in their 40s. The overall prevalence was 17.08%. Subjects with corrective saccades exhibit lower VOR gain than those without it (p < 0.001). Age, sex, hypertriglyceridemia, and hearing levels at 4000 Hz were significantly associated with the presence of corrective saccades.
Conclusion
Vestibular function declined with age, influenced significantly by sex, hypertriglyceridemia, and hearing level at 4000 Hz. The increased prevalence of corrective saccades among older adults underscores the importance of early detection and intervention. Understanding age-related changes in vestibular function can facilitate appropriate management strategies and countermeasures at the personal and societal healthcare level.
Introduction
The vestibulo-ocular reflex (VOR) is a critical reflex that helps maintain balance by causing the eyes to move at the same speed but in the opposite direction of head movements. This mechanism ensures stable visual perception of objects even during body motion. Historically, techniques such as the rotating chair and caloric tests were used to evaluate the VOR. However, these methods were complex, time-intensive, and involved rotational stimulation at lower frequencies than those experienced during typical daily head movements. The video head impulse test (vHIT) was developed to address these limitations, which has since proven effective in evaluating many patients with vestibular dysfunction. 1 The vHIT objectively assesses the presence of peripheral vestibular impairment by evaluating the VOR.2,3 The VOR is among the fastest reflexes in the human body, with a latency of <8 ms. Unlike earlier techniques, the vHIT efficiently evaluates high-frequency head movements in the 1–5 Hz range, corresponding more closely to the frequencies of natural head movements in daily life. 4
Since most tests are performed on patients who attend the hospital due to vertigo, limited studies investigate VOR in the general population. Carol et al. studied 109 participants aged 26–92 years who were free from vestibular symptoms and found that seven participants (6.4%) had VOR gains <0.8. Their analysis revealed that VOR gain remained stable from age 26 to 79, after which it declined significantly at a rate of 0.016/year. 5 Yang et al. examined the VOR in 50 healthy participants aged 20–69 years. While the number of participants with VOR gains <0.8 was not reported, they observed that 22.6% of head impulse trials showed catch-up saccades. Their data indicated no differences in VOR gain across age groups. However, it aligned with previous findings that VOR gain is stable until age 70, after which it decreases. 6 Mossman et al. investigated VOR gain in 60 healthy participants aged 20–80 years. By analyzing data from both eyes, they found that 2–4 participants (1.7%–3.3%) had VOR gains <0.8, depending on VOR frequencies. Unlike the previous studies, they proposed a consistent decline in VOR gain of 0.012–0.017 per decade with advancing age. 7
These studies concur that abnormal VOR can occur even in asymptomatic healthy participants and that VOR gain decreases with age. However, they did not consider other factors that may influence VOR. While the factors affecting VOR are not yet fully elucidated, previous research suggests the involvement of potential contributors. Nakamichi et al. compared VOR gain between participants with sudden hearing loss accompanied by vertigo and those with vestibular neuritis, revealing significant differences. 8 This finding aligns with the results of Nam et al. and Liu et al., who highlighted the influence of hearing loss on VOR gain.9,10 Similarly, Say et al. emphasized the role of hearing loss by comparing VOR gain in patients with presbycusis to that of age-matched normal controls. The caloric test results were comparable between both groups; however, VOR gain was significantly lower in the presbycusis group. 11 Additionally, research has indicated that tinnitus and vision may also impact VOR.12,13 While evidence increasingly supports the notion that VOR is influenced by various factors, comprehensive studies exploring the combined effects of age, hearing abilities, and other chronic conditions on VOR in the general population remain limited.
Since 1998, the Korean National Health and Nutrition Examination Survey (KNHANES) has been conducted by the Disease Control Headquarters to generate nationwide statistics on the health and nutritional statuses of Koreans. This survey comprises a health interview, nutritional survey, and health examination conducted via household interviews or direct physical examinations by professionals. KNHANES has proven to be a valuable resource for assessing the national prevalence of specific diseases and health behaviors within the general population. The vHIT, known for its convenience and effectiveness in assessing vestibular function, has been included in KNHANES since 2019. To our knowledge, this is the first national epidemiological survey worldwide to evaluate vestibular function quantitatively. This study aimed to investigate age-related changes in vestibular function in the general population using 2021 KNHANES data and to evaluate the impact of hearing abilities and other potential factors on VOR.
Materials and methods
Study design and participants
This study utilized data from the KNHANES conducted by the Disease Control Headquarters. The 2021 cohort was surveyed following a two-stage clustered (region and household) and stratified random sampling method, ensuring a representative sample of the entire Korean population. Participants included in this study were those over 40 years of age who had completed the vHIT and a hearing assessment using pure-tone audiometry. The institutional review board of Incheon St. Mary’s Hospital of the Catholic University of Korea (OC23ZASI0162) approved this study.
Clinical and laboratory measurements
Health-related variables, biochemical measurements, and economic and educational status were included in the analysis. Blood pressure was measured three times in the sitting position after a 5-min rest, and the average of the second and third readings was used for analysis. Hypertension was defined as systolic BP ≥ 140 mmHg, diastolic BP ≥ 90 mmHg, or the use of antihypertensive medication. Prehypertension was defined as systolic pressure between 120 and 139 mmHg or diastolic pressure between 80 and 89 mmHg. Normal blood pressure was defined as systolic BP < 120 mmHg and diastolic BP < 80 mmHg.
Fasting blood glucose (FBG), glycosylated hemoglobin (HbA1c), triglyceride (TG), and total cholesterol (TC) levels were measured after overnight fasting. Diabetes was defined as follows: (1) FBG level ≥126 mg/dL, (2) a diagnosis of diabetes by a medical professional, or (3) the use of oral hypoglycemic agents or insulin injections. Prediabetes was defined as follows: (1) FBG level between 100 and 125 mg/dL or (2) HbA1c level between 5.7% and 6.4%. Normal glucose levels were defined as (1) FBG <100 mg/dL or (2) HbA1c < 5.7%. Hypercholesterolemia was defined as TC ≥ 240 mg/dL or the use of cholesterol-lowering medications. Hypertriglyceridemia was defined as TG ≥ 200 mg/dL.
Smoking status was categorized based on lifetime experience: (1) never smoked, (2) smoked less than five packs, and (3) smoked more than five packs. Alcohol consumption was classified into four categories: (1) No alcohol consumption (defined as never consuming alcohol), (2) drinking alcohol 1–4 times a month, (3) drinking alcohol 2–3 times a week, and (4) drinking alcohol more than 4 times a week. Average household income was calculated based on the median income of the study participants and categorized into four groups: low, lower middle, upper middle, and high. Finally, education status was classified into four levels: elementary school, middle school, high school, and college.
Vestibular function evaluation
Otolaryngology-related variables from the KNHANES items are being jointly investigated with the Korean Society of Otorhinolaryngology-Head and Neck Surgery. The vHIT was administered to participants aged over 40 years. Trained audiologists performed the vHIT, with quality control supervised by society executives and current university faculty members. A vHIT device from GN Otometrics (ICS Impulse; GN Otometrics, Taastrup, Denmark) was used to record eye movements, and default software settings were applied.
The average bilateral VOR gain and the presence of corrective saccades were calculated for each participant. To exclude participants with potential previously impaired vestibular function, such as those with prior vestibular neuritis or Meniere’s disease, samples showing average VOR gains <0.8 and a gain difference of >10% between sides were excluded.14,15 Additionally, if the gain value of either side exceeded 1.2, it was considered indicative of goggle slippage and excluded from the analysis. Corrective saccades were identified if they occurred at least twice on one side. Finally, the participants were divided into the normal vestibular function group and the normal VOR gain with corrective saccades group (normal VOR gain with CS group) for analysis.
Audiometric evaluation
The hearing threshold was assessed by trained audiologists using an automatic audiometer (GSI SA-203, Entomed Diagnostics AB, Lena Nodin, Sweden) in a soundproof booth. Thresholds were measured at frequencies of 0.5, 1, 2, 4, and 8 kHz for both ears. The pure-tone average (PTA) was calculated as the mean of the pure-tone thresholds at 0.5, 1, 2, and 4 kHz. To exclude individuals with pathologically impaired hearing, such as chronic otitis media or sudden hearing loss, the PTA of each ear was compared, and the ear with the better hearing level was selected for analysis.
Statistical analysis
All statistical analyses were performed using Statistical Package for the Social Sciences software version 21 for Windows (IBM Corp., Armonk, NY, USA). Descriptive statistics were presented as the mean and standard deviation. Comparisons between the normal and abnormal vestibular function groups were conducted using t-tests and chi-squared tests. Multiple regression analysis was used to predict the association between vHIT results and hearing levels or other demographic factors. Additionally, a simple regression analysis was initially performed to identify potential causative factors influencing vestibular dysfunction. The multiple regression model subsequently included variables identified as potentially significant in the simple regression analysis. A p-value <0.05 was considered statistically significant.
Results
Study population
Of the 7090 participants who took part in the 2021 KNHANES, 4853 were excluded due to missing vHIT data. This exclusion included 2657 participants under the age of 40 who were not eligible for vHIT and 2196 participants who did not undergo vHIT due to reasons such as refusal, lack of cooperation, or a history of cervical disc herniation. Of the remaining 2237 participants who underwent vHIT, 187 were excluded due to missing demographic or audiometric data, 346 were excluded due to goggle slippage (VOR gain >1.2), 59 were excluded due to possible bilateral vestibulopathy (VOR gain <0.8), and 375 were excluded due to possible unilateral vestibulopathy (a gain difference <10% between sides).
In total, 1270 participants were included in the final analysis. Notably, among these 1270 participants, 607 were men (Figure 1). The age distribution was as follows: 449 participants aged 40–49, 380 aged 50–59, 288 aged 60–69, and 153 aged 70–80 (Table 1). Participant flow and data analysis in the study. Prevalence of vestibular dysfunction according to age. VOR, vestibulo-ocular reflex; OR, odds ratio; CI, confidence interval.
Vestibular function according to age
Vestibular function was analyzed according to age. We assessed vestibular function using two metrics: the VOR gain and the presence of two or more corrective saccades.
When assessing the VOR gain, we found that it decreased with age. However, it was not statistically significant (coefficient −0.0003, p = 0.281). Based on previous reports, we further analyzed the trend of VOR gain decline after the age of 70. Nevertheless, no statistically significant differences were found between VOR gain and age in the 40–70 age group (coefficient −0.0002, p = 0.58) and after the age of 70 (coefficient 0.0006, p = 0.783). The average VOR gain values by age group were as follows: 1.04 (40–49 years), 1.04 (50–59 years), 1.03 (60–69 years), and 1.02 (70–80 years; Table 1).
We analyzed the presence of corrective saccades and found that their prevalence increased with age. Corrective saccades were observed in 9.97% of participants in their 40s, 17.6% in their 50s, 20.1% in their 60s, and 30.7% in their 70s. Statistical analysis confirmed that corrective saccades became significantly more prevalent with increasing age, with participants in their 70s being 3.98 times more likely to exhibit corrective saccades than those in their 40s (Table 1).
Comparison between the normal vestibular function group and the normal VOR gain with CS group
Comparison between the normal vestibular function group and the normal VOR gain with CS group.
aThe Shapiro–Wilk test indicated that the VOR gain did not follow a normal distribution; therefore, the Wilcoxon rank-sum test was used for group comparison. Accordingly, the results were reported as median and interquartile range (IQR) due to the non-normal distribution of the data.
The VOR gain significantly differed between the groups, with a mean value of 1.01 ± 0.11 in the normal VOR gain with CS group compared to 1.04 ± 0.14 in the normal vestibular function group (p < 0.001). Significant differences were observed in age, sex, educational status, income level, and hearing levels. The normal VOR gain with CS group was older (59.7 ± 10.9 years) than the normal vestibular function group (54.6 ± 10.3 years). A significantly higher proportion of males was observed in the normal VOR gain with CS group (p < 0.001). Age was evenly distributed in the normal VOR gain with CS group, whereas individuals in their 40s predominated the normal vestibular function group. Educational status and income level significantly differed between the groups, with the normal vestibular function group having higher levels in both variables.
Other health-related variables, such as the presence of hypertension, diabetes mellitus, hypercholesterolemia, and hypertriglyceridemia, were higher in the normal VOR gain with CS group; however, no statistically significant differences were observed. Smoking and alcohol consumption were comparable between the groups. Hearing levels were analyzed across each frequency and were worse in the normal VOR gain with CS group compared to the normal group for all frequencies.
Factors associated with the presence of corrective saccades
Possible associated factors on vestibular function.
Discussion
The present study aimed to identify age-related changes in vestibular function in the general population and explore possible associated factors. The main findings can be summarized as follows: First, the VOR gain remained constant with age. Second, the presence of corrective saccades increased with age. Third, a few factors, age, sex, hypertriglyceridemia, and hearing level at 4000 Hz, influenced the presence of corrective saccades.
This study utilized vHIT data from adults over 40 years of age from the KNHANES dataset to evaluate vestibular function. It is a meaningful contribution as it confirmed quantitative changes in vestibular function within the general population rather than in patients seeking care for dizziness. Furthermore, excluding data with potential testing errors (e.g., goggle slippage) and previously impaired vestibular function, such as those with prior vestibular neuritis or Meniere’s disease, allowed for a more accurate assessment of aging-related changes in vestibular function. In particular, samples showing a gain difference of >10% between sides were excluded to eliminate cases with possible prior unilateral vestibulopathies. When a vestibular function is impaired, the VOR gain may partially recover up to 0.8 over time; however, not entirely.16,17 Consequently, including the partially recovered subjects could result in an overestimation of vestibular dysfunction prevalence with age and may fail to accurately reflect the effects of aging alone.
We found that the VOR gain stayed constant with age when excluding individuals with potential testing errors and previously impaired vestibular function. Moreover, some studies have analyzed age-related vestibular function using VOR gain, and they yielded diverse results. One study reported no changes in VOR gain with age, 6 another observed a continuous decline in VOR gain with age, 7 and the other found that VOR gain remained stable until approximately age 70, after which it declined rapidly.5,18 In our study, the VOR gain showed a decreasing trend with age; however, it did not reach statistical significance. Additionally, no meaningful difference was found when further analysis was performed based on age 70. This discrepancy is likely due to differences in subject selection, as we excluded individuals with potential test errors and prior impaired vestibular dysfunction. These exclusions likely minimized the phenomenon of cumulative vestibular damage in older participants caused by prior pathology.
Unlike VOR gain, the presence of corrective saccades increased with age. The overall prevalence of corrective saccades was 17.08%, with 9.97% and 30.7% of participants aged 40–49 and 70–80 years, respectively, showing corrective saccades despite normal VOR gain. Both the VOR gain <0.8 and the presence of corrective saccades are signs of impaired vestibular function. Previous studies have shown that the presence of corrective saccades reflects impaired vestibular function more sensitively than the VOR gain.19–21 Moreover, even when vestibular function is restored and the VOR gain increases, corrective saccades often persist.20–22 Thus, the observed increase in corrective saccades with age in this study may indicate that vestibular function declines with age. It is also supported by the finding that the VOR gain was significantly lower in the normal VOR gain with CS group compared to the normal vestibular function group. However, the interpretation requires caution. While the examiners identified it as a corrective saccade, it could also be an artifact (e.g., due to blinking) or a square wave jerk. Square wave jerks reportedly occur in 24%–60% of healthy adults, 23 and they are more common in older adults. 24 While many of these cases were found to be preceded by peripheral vestibular pathology, 25 it can be either a nonspecific sign or a valuable sign in neurological and psychiatric disorders. 26
From the analysis, we found that age, sex, hypertriglyceridemia, and hearing threshold at 4000 Hz were the factors with a significant effect on the presence of corrective saccades. The likelihood of having corrective saccades increases by 1.052 times for every one-year increase in age. This finding parallels the progression of age-related hearing loss in the ear. The semicircular canals, responsible for transmitting head angular acceleration, undergo degeneration with aging, which is a major factor contributing to the general degradation of the vestibular system. 27 The crista ampullaris, serving as the receptor for the angular VOR, is composed of hair cells and supporting cells. Previous research has shown that vestibular sensory and supporting cells in humans undergo age-related changes, including reduced hair cell numbers, the presence of lipofuscin inclusions, and cilia deformation. 28 Quantitative assessments of vestibular hair cells across different ages have revealed a 40% reduction in older individuals compared to younger individuals. 29 These age-related changes are likely the primary reason for the increased prevalence of corrective saccades with advancing age.
We also observed a higher association of prevalent corrective saccades with males. This finding is particularly noteworthy, as it contrasts with existing literature, where women are more frequently affected by specific vestibular disorders such as benign paroxysmal positional vertigo and vestibular migraine.30,31 However, a study indicates that although women are generally overrepresented in the incidence of many vestibular disorders, men might exhibit higher instances of specific types of vestibular dysfunction in certain aspects. This includes potential differences in response to neuropharmacological agents due to inherent neurochemical differences between males and females, which could influence the manifestation of vestibular dysfunction differently across sexes. 32 Another study suggested that hormones, including testosterone, affect vestibular function, as receptors for these hormones are present in the inner ear and along vestibular pathways. 33 This suggests that hormonal fluctuations could significantly influence vestibular health. It is commonly recognized that vestibular issues are more prevalent among females; however, the evidence suggests that male-specific vestibular dysfunctions may also exist but are less recognized or underreported. Therefore, further research is necessary to fully understand the impact of sex on vestibular function and uncover the complete spectrum of vestibular disorders across sexes.
Our study revealed that elevated triglyceride levels were associated with an increased risk of having corrective saccades, with an odds ratio of 1.62 (p < 0.05). This correlation may be attributed to the impact of hypertriglyceridemia on microcirculation, particularly within the vertebrobasilar system, which supplies blood to structures, including the inner ear. The disruption in microvascular blood flow could lead to ischemia of the vestibular organs, thereby impairing their function.34,35 Previous research supports this hypothesis, suggesting that cardiovascular risk factors, including dyslipidemia, can affect vestibular function through similar mechanisms that lead to cochlear blood flow impairment.36,37
A hearing level of 4000 Hz was associated with the presence of corrective saccades; every 10 dB increase in the hearing level of 4000 Hz increased the likelihood of having corrective saccades by 1.052 times. It was a notable and interesting finding that not the hearing level at 8000 Hz but at 4000 Hz was associated with vestibular function since the hearing loss at higher frequencies is more associated with age-related changes, and the higher frequencies are anatomically closer to the vestibular organ. This was not mentioned in the manuscript; however, we also analyzed the factors that affect hearing levels in reverse. It revealed that neither the VOR gain nor the presence of corrective saccades was associated with the hearing level (Supplement 1). Moreover, while both the auditory and vestibular functions showed a decline with age, the rate of decline was significantly different. These findings would suggest that the two organs are independent regarding functional deterioration. It is supported by a study examining hair cell changes following occlusion of the major vascular supply to the inner ear in mice. 38 Anatomically, the auditory and vestibular organs share several structures and are susceptible to similar pathological processes. However, the study revealed that either temporary or permanent arterial occlusion resulted in significantly greater hair cell loss in the cochlea than in the vestibule. Additionally, the vestibular organ can replace a small number of lost hair cells, whereas the cochlea does not. 39 Research has observed that stem cells in the cochlea decrease significantly by the second to third postnatal weeks, while those in the vestibule remain constant or even increase. The reason for this difference is unknown, although studies have shown the distinct features of functional deterioration in the two organs. However, the association between the hearing level at 4000 Hz and vestibular function remains questionable. Since regression analysis does not establish causality, other factors, such as noise exposure, may influence this finding, impairing both hearing level at 4000 Hz and vestibular function. Animal models have confirmed a dose-dependent decline in vestibular function following noise exposure. 40 Consequently, exposure to the identical cause may have yielded analogous outcomes.
This study has several limitations. Firstly, although individuals with suspected previously impaired vestibular function were excluded, it cannot be guaranteed that all such individuals were removed from the sample. Corrective saccades often remain even when the VOR gain recovers. Consequently, when corrective saccades are observed with normal VOR gain, it becomes difficult to ascertain whether this results from age-related vestibular function deterioration or a partial restoration of previously impaired vestibular function. Secondly, the proficiency of the examiners with the equipment and the compliance of participants may have influenced the outcomes. Field surveyors underwent at least six hands-on training sessions before the survey, and data were only included if they met quality criteria in five domains: goggle and camera preparation, calibration, head rotation trajectory and speed, data recording, and interpretation. Two interim quality checks were conducted to ensure data reliability. Although the vHIT test was performed under the above strict criteria, it is a test influenced by head velocity, which means the results may have been affected by the examiner or the participants. Furthermore, while the identification of “corrective saccades” was carefully performed by trained audiologists and supervised by university faculty, we acknowledge that this metric may still include artifacts or other non-specific findings. Lastly, although this study aimed to analyze the influence of individual health-related variables on vestibular function, environmental factors such as noise exposure were not included. Noise exposure is a recognized factor that can affect vestibular function, and its influence is more emphasized by the results that the presence of corrective saccades was associated with the hearing level at 4000 Hz. It necessitates future research on this effect.
While the present study has some limitations, its large general population sample makes it meaningful. This study confirmed age-related changes in vestibular function, which were observed to decline consistently with age. Balance disorders have implications that extend beyond falls, as they are now known to be highly associated with an increased risk of all-cause mortality, as well as cardiovascular disease and cancer mortality. 41 Understanding these age-related changes in vestibular function could aid in developing proper management strategies and countermeasures at both personal and societal levels of healthcare.
Supplemental Material
Supplemental Material - Which factors influence the deterioration in vestibular function? A nationwide, population-based study with video-head impulse test
Supplemental Material for Which factors influence the deterioration in vestibular function? A nationwide, population-based study with video-head impulse test by Jeon Mi Lee, Sung Goo Yoo, and Hyun Jin Lee in Journal of Vestibular Research.
Footnotes
Funding
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. RS-2022-NR073383) to J.M.L. This work was supported by the NRF grant funded by the Korean government (MIST) (No. RS-2023-00210073) to H.J.L.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Supplemental Material
Supplemental material for this article is available online.
References
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
