|Year : 2018 | Volume
| Issue : 3 | Page : 172-178
Does postural instability in type 2 diabetes relate to vestibular function?
Marniza Omar1, Nor Haniza Abdul Wahat2, Mohd Fawwaz Afif Zulkafli1, Nur Fajarina Husain1, Suhaina Sulaiman1
1 Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia
2 Faculty of Health Sciences, Universiti Kebangsaan Malaysia; Institute of Ear, Hearing & Speech (INSTITUTE-HEARS), Kuala Lumpur, Malaysia
|Date of Web Publication||11-Jan-2019|
Dr. Nor Haniza Abdul Wahat
Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur
Source of Support: None, Conflict of Interest: None
Introduction: Diabetes mellitus (DM) can lead to complications including postural instability that may be related to impaired function of the vestibular system. Aims and Objectives: This study aims to measure vestibular and balance function in adults diagnosed with type 2 noninsulin-dependent diabetes mellitus (NIDDM) and to compare their findings with healthy age-matched control group. Materials and Methods: This is an experimental cross-sectional study, using purposive sampling method. Eight NIDDM patients (mean age = 36.8 ± 11.4 years) and eight age-matched healthy controls (mean age = 34.6 ± 11.0 years) were recruited. Vestibular end organs (i.e., saccule, utricle, and semicircular canals) were assessed using cervical and ocular vestibular-evoked myogenic potentials (cVEMPs and oVEMPs) and video head impulse test. Upright stance postural stability was assessed using force plate in four testing conditions, i.e., standing on firm or foam surface with eyes opened or closed. Dynamic stability was measured using Timed Up and Go (TUG) and functional gait assessment (FGA). Results: There was no statistically significant difference for all vestibular tests between groups. However, reduced p13-n23 interamplitudes (for cVEMPs) and n10 amplitudes (for oVEMPs) were observed in NIDDM patients. Upright stance postural stability was not significantly worse in patients. For dynamic postural stability, NIDDM patients demonstrated significantly poor performance in TUG and FGA than the healthy controls. Functionally, NIDDM patients walked significantly slower and less stable, and this is evident from poor performance in both TUG and FGA results. Conclusion: Our findings showed significant reduction in dynamic postural stability in NIDDM patients. However, we did not find any significant abnormal vestibular function in the patients as reported by previous studies. Further research studies are advocated.
Keywords: Diabetes mellitus, functional gait assessment, timed up and go, vestibular-evoked myogenic potentials, video head impulse test
|How to cite this article:|
Omar M, Abdul Wahat NH, Zulkafli MF, Husain NF, Sulaiman S. Does postural instability in type 2 diabetes relate to vestibular function?. Indian J Otol 2018;24:172-8
|How to cite this URL:|
Omar M, Abdul Wahat NH, Zulkafli MF, Husain NF, Sulaiman S. Does postural instability in type 2 diabetes relate to vestibular function?. Indian J Otol [serial online] 2018 [cited 2019 Jan 18];24:172-8. Available from: http://www.indianjotol.org/text.asp?2018/24/3/172/249869
| Introduction|| |
The prevalence of diabetes is reportedly increasing across countries in the world. According to the National Health and Morbidity Survey in Malaysia, the prevalence of diabetes mellitus (DM) increased from 11.6% to 17.5% for the year 2006–2015. Possible factors that contribute to increment in diabetic prevalence in Malaysia include unhealthy life-style, aging community, and urbanization., Diabetes can cause one or more health problems including microvascular (e.g., diabetic nephropathy, neuropathy, and retinopathy) and macrovascular complications (e.g., coronary artery disease, peripheral arterial disease, and stroke).,
Increased utricle and saccule vascularization in mice induced by DM has been reported. It was suggested that vascularization may possibly reduce oxygen supply to the affected organs. Oxygen reduction will later cause degeneration of type I vestibular hair cells, which eventually affects the vestibular function. A study in human reported that 53.3% from 15 patients with type 2 DM have abnormal cervical vestibular-evoked myogenic potentials (cVEMPs), indicating abnormal saccule function. This result is supported by an animal study, which reported degeneration of type I vestibular hair cells in the saccular neuroepithelium. Impaired diffusion of oxygen, nutrients, and waste material through the dense extracellular matrix were reported to be the possible caused for the degeneration of vestibular hair cells. Ward conducted a study on the impact of diabetes on three semicircular canals (SCCs) using head thrust dynamic visual acuity test. The result showed that 70% of 25 patients with type 2 DM have an abnormal response at least in one of the three SCCs.
Findings from the aforementioned studies indicated that the prevalence of vestibular impairment is high in diabetic patients. Hence, higher risk of postural instability and falls maybe further increased because of vestibular dysfunction. Impaired postural control particularly during gait has been reported in diabetic patients., Change in gait characteristics (i.e., reduced gait speed and shorter steps with a wider step width) in type 2 DM patients has been documented. Brach et al. investigated possible explanatory causes for gait impairment in diabetic patients. The authors reported health status and lower extremity strength contributed greatest proportion to the association between DM and gait speed. The study also found that DM was related to step width; however, the association cannot be explained by other factors related to balance such as peripheral sensation, lower extremity strength, and vision. The authors suggested that changes in step width noted in diabetic patients may be contributed by vestibular organs. Damage to these systems has been found to be associated with impaired microcirculation due to poor glucose control in diabetic patients. Morphological and physiological changes were also found in animal induced with DM.
To the best of our knowledge, there is paucity of study that includes comprehensive vestibular and balance assessments in diabetic patients. Thus, this study aimed to investigate the vestibular end organ function and postural stability in type 2 noninsulin-dependent diabetes mellitus (NIDDM) patients, using a set of vestibular test battery and balance assessments. These will enable objective quantification of vestibular and balance function in NIDDM patients. Abdul Wahat et al. first described the prevalence of vestibular disorders in a tertiary referral hospital in Malaysia. Following this study, it is also of our interest to determine the vestibular performance of NIDDM patients from similar hospital setting.
| Materials and Methods|| |
This cross-sectional study was conducted on NIDDM patients (mean age: 36.8 ± 11.4 years) and age-matched control group (mean age: 34.6 ± 11.0 years). The NIDDM patients were recruited from a tertiary referral hospital based on these inclusion criteria: (i) diagnosed with type 2 DM for the period of 5 years or less, (ii) noninsulin-dependent, and (iii) able to stand and walk independently. Patients diagnosed for 5 years or less were recruited because we want to exclude any possible diabetic complications that may cause neuropathy. The following inclusion criteria were employed for the control group: (i) no history of vertigo or balance problem and (ii) no other significant medical history that may affect postural stability. All participants were excluded if they have (i) hearing loss, (ii) history of other pathology or conditions that may affect central nervous system, (iii) musculoskeletal conditions that would impair gait and balance, and (iv) chronic vision problem. In total, 16 subjects participated in this study (n = 8 for each group). Written consent was obtained from all participating subjects. This study was approved by the institution ethical committees.
Vestibular and balance assessments
Three assessments employed for the peripheral vestibular systems were cVEMPs, ocular vestibular-evoked myogenic potentials (oVEMPs), and video head impulse test (vHIT). Dynamic postural stability was measured using functional gait assessment (FGA) and timed up and go (TUG). Force plate Balance Rehabilitation Unit (Medicaa, Monte-video, Uruguay) was used to measure postural stability in static condition. All assessments were conducted in random order.
Cervical vestibular-evoked myogenic potentials and ocular vestibular-evoked myogenic potentials
Saccule and utricle function was assessed using cVEMPs and oVEMPs consecutively. Eclipse EP25 (Interacoustics, Denmark) was used to measure both cVEMPs and oVEMPs. Both tests were conducted using 750-Hz tone burst acoustic stimulation, with condensation polarity (rise/fall time 0 ms; plateau 2.67 ms). The stimulation rate was 5/s, with 50-ms time window. The electromyography (EMG) was amplified and bandpass filtered between 20 and 2000 Hz (for cVEMPs) and between 20 and 500 Hz (for oVEMPs). The cVEMP stimuli were presented at 100 dBSPL through ER3A insert earphones and averaged over 150 stimuli for each run. oVEMPs were presented at 50 dBnHL through Brüel and Kjær (B and K) (Naerum, Denmark) mini-shaker 4810 and averaged over 80 stimuli for each run. The mini-shaker was fitted with a short M4 bolt (2 cm in length) terminated in a bakelite cap and placed on Fz (i.e., at the very high forehead position) during the stimulation and recording.
Subject was instructed to sit-up right on a static chair. For cVEMPs, active electrodes were placed on the skin over the midpoint of the sternocleidomastoid (SCM) muscle on each side of the neck, reference electrode on the clavicle bone, and ground electrode on the sternum. Subjects were then instructed to turn their head to the left and right, contracting the ipsilateral SCM muscle. EMG meter together with visual and acoustic monitoring was used to make sure optimal SCM muscle contraction. For oVEMPs, active electrodes were positioned on the skin over the infraorbital ridge and reference electrode was placed 2 cm below the active electrode, while the ground electrode on the chin. The active and reference electrodes on each side of the eye were positioned to be in line with the middle of the pupil when the subject looked up. Before the test begins, the subject was instructed to look to the center and upward. The electrodes' impedance was kept below 5kΩ. The recording and stimulation methods were conducted based on the protocol proposed by Abdullah et al.
cVEMPs and oVEMPs were considered present when there were repeatable and reproducible waveforms elicited. Parameters recorded for cVEMPs were p13 and n23 latencies and p13-n23 interamplitude. For oVEMPs, the measured parameters were n10 latency and peak-to-base amplitude.
Video head impulse test
The function of all six SCCs was assessed using vHIT, through the EyeSeeCam system (Interacoustics, Denmark). Subject seated on a static chair, 1.5 m from a visual target. A pair of lightweight goggle mounted with a built-in video camera and motion sensor was utilized to record eye and head movements, respectively. Calibration was done before testing, to ensure appropriate head and eye measurements. Head impulses were delivered randomly with brief, abrupt head turns in the plane of each SCC (lateral, anterior, and posterior). The vertical testing was done accordingly with matched pairs of the SCC; left anterior–right posterior and right anterior–left posterior.
Twenty averages were obtained for each SCC for the left and right ears. Recorded responses (i.e., the vestibulo–ocular reflex [VOR] gain) were automatically calculated by the software. The VOR gain is defined as the ratio of eye velocity to head velocity. Appearance of any saccade was also documented.
Static postural assessment
Sway velocity (SV, cm/s) was measured during quiet stance on a 40 cm × 40 cm force platform. Testing conditions were standing on firm or foam surface, with eyes opened (EO) or closed (EC). The foam was placed on the force platform. Each testing condition lasted for 30s. All conditions were performed in the same order for all participants.
Dynamic postural assessment (functional gait assessment and timed up and go)
FGA is a ten-item test, specially developed for patients with vestibular disorders, based on the dynamic gait index. Its purpose is to assess postural stability during various walking tasks which include walking with head movements, tandem, or backwards. Each item is rated between 0 (severe impairment) and 3 (normal) with a maximum score of 30; higher scores indicate better performance. For adults up to 60 years old, the normal score on the FGA would be considered >27/30.
TUG aimed to assess subject's functional mobility. It measures the time (in seconds) required for a person to stand up from a chair, walked for three meters at their normal speed, and turned back to the chair and sit down. This test is commonly used to evaluate the dynamic balance and individuals at risk for falls (i.e., older adults and patients with vestibular impairments or neurological diseases).,, Higher scores indicate poor balance and increased risks for falls.
The IBM Statistical Package for the Social Sciences, version 21 (SPSS Inc., Chicago, Illinois, USA) was used to analyze the obtained data. For normally distributed data, an independent t-test was used to compare between ears and between-group differences. For nonnormally distributed, a Mann–Whitney U-test was performed. P < 0.05 was considered to be statistically significant.
| Results|| |
Cervical vestibular-evoked myogenic potentials and ocular vestibular-evoked myogenic potentials
Mean, standard deviation (SD), and range of responses (minimum–maximum) for n10 latency and peak-to-base amplitude for oVEMPs, and p13, n23 latencies, and peak-to-peak amplitude for cVEMPs were shown in [Table 1]. Independent t-test showed no statistically significant ear effects for the oVEMPs' n10 latency and amplitude, as well as the cVEMPs' p13, n23 latencies, and amplitudes in both groups. The responses were then collapsed resulting in a maximum of 16 ears for each group.
|Table 1: Mean latencies and amplitudes for ocular vestibular-evoked myogenic potentials and cervical vestibular-evoked myogenic potentials in the control and noninsulin-dependent diabetes mellitus (NIDDM) groups|
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For oVEMPs, no significant differences (P > 0.05) were found for both n10 latency and peak-to-base amplitude between healthy control and NIDDM groups. However, the mean peak-to-base amplitude for NIDDM was observably reduced compared to controls.
We also observed reduction in cVEMPs' interamplitude (ranged between 29.00 and 78.02 μV) in NIDDM patients compared to healthy controls (ranged between 36.65 and 104.20 μV), although the difference was not statistically significant (P > 0.05) for both amplitudes and latencies. Absence cVEMPs' responses were noted in two diabetic patients. An example of the absent response was shown [[Figure 1]a; NIDDM patient, S1].
|Figure 1: Responses obtained on the right ear from an age-matched subject (control) and a noninsulin-dependent diabetes mellitus (NIDDM) patient (S1). Top (a) cervical vestibular-evoked myogenic potentials traces, with labeled p13 and n23 for a control and absence peak(s) for S1. Bottom (b) mean ± standard deviation for lateral video head impulse test instantaneous gain measured at 60 ms. S1 scored very low gain (0.52) as compared to the control (1.11)|
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Video head impulse test
Comparison between ears within a group showed significant results for the anterior SCC (controls: t (14) = −2.67, P = 0.02; DM: t (14) = −3.17, P = 0.01) and posterior SCC (controls: t (14) =5.11, P = 0.00; DM: t (14) =3.83, P = 0.00). Thus, the results were analyzed separately, i.e., right and left ears. No significant difference (P > 0.05) was found for the VOR gain for all SCCs between groups. Overt and covert saccades were not present in all participants. The mean (±SD) for the VOR gain for all SCCs were shown in [Table 2]. We observed two NIDDM patients with either abnormally low or high VOR instantaneous gain in either one of the SCC. A comparison example of the VOR gain in a NIDDM patient (i.e., S1) and a healthy control was shown in [Figure 1]b.
|Table 2: Mean vestibule-ocular reflex gain for all semicircular canals in the control and noninsulin dependent diabetes mellitus (NIDDM) groups|
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Significant between-group differences were noted for both FGA and TUG. Patients scored higher (i.e., worse) in TUG [t (14) = −4.59; P = 0.00] and scored lower (i.e., worse) in FGA [z = −2.91; P = 0.00]. Findings on static balance tasks were not significantly different between groups, suggesting that NIDDM patients did not sway more than healthy control during quiet stance tasks. Descriptive data for balance outcomes were shown in [Table 3].
|Table 3: Mean sway velocity, timed up and go, and functional gait assessment in the control and noninsulin-dependent diabetes mellitus (NIDDM) groups|
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| Discussion|| |
This study showed no significant between-group differences in all vestibular assessments. Previous studies on cVEMPs and oVEMPs revealed inconsistent outcomes. Kalkan et al. reported no significant difference in VEMP latencies between healthy control and DM groups, while other study reported delayed latencies in approximately 50% of type 2 DM patients., Reduced VEMP amplitudes were consistently reported in previous studies.,, Saccule was reported to be more susceptible to diabetes which may contribute to the changes in amplitude and latency of VEMPs. It was thought that the abnormal cVEMPs' responses were due to degeneration of type 1 vestibular hair cells. These hair cells were more susceptible to ototoxic medications compared to type 2 vestibular hair cells. The damage on small blood arteries prevents the oxygen and nutrients supply to the vestibular apparatus and led to vestibular dysfunction., It was believed that the damage on the vestibular hair cells was due to metabolic changes and reduced oxygenation to the vestibular apparatus.,,
To the best of our knowledge, one study reported vHIT findings among DM patients. Kalkan et al. reported no significant difference of vHIT responses between healthy controls and DM patients. They also reported that none of the patients showed overt or covert saccades in vHIT analyses. These results are in line with our findings.
Impaired postural control and gait alteration were also reported in DM patients. Reduced postural stability and impaired gait due to peripheral neuropathy are the most common DM complications that may lead to increase risk of falls in patients. Studies reported higher risk of severe injuries and fracture after a fall in older adults with DM than those without., In the present study, high TUG score (indicating slower walking speed) and low FGA score (indicating reduced stability) were noted in NIDDM patients. These are consistent with earlier studies., In the present study, the average TUG score for NIDDM patients (i.e., 12.57 s) exceeded the fall risk cutoff score of 12 s that was proposed for community-dwelling older adults. This suggested poor dynamic functional balance among participated NIDDM patients considering their younger age range, i.e., 21–55 years. Although this study was not able to demonstrate significant vestibular dysfunction in diabetic patients, the role of vestibular system in postural and gait control in patients cannot be undermined.
An earlier study reported impaired hip and knee joint movements as objectively recorded by accelerometers in DM patients. The accelerometers' data suggested greater joint tremors during flexion–extension and greater joint movements during gait in DM patients compared to healthy control. These imply motor control deficit at the joints, and these changes were not contributed by muscles strength or sensory loss at foot. The authors proposed alteration in gait characteristics and motor control at joints could be linked to either reduction of peripheral or central-reflex control. The involvement of these reflexes has direct linkage with impaired vestibular reflexes from lack of arterial circulation.
In our study, SV during static balance tasks was not significantly different between groups. However, there was a pattern in which DM patients have greater sway in almost all conditions, suggesting instability during quiet standing with EO or EC. More challenging tasks such as tandem stance or dual-task balance tests may be required to detect differences between groups.
Previous studies reported greater sway in DM patients and the sway was worse in the presence of neuropathy or when visual input was eliminated., A study was conducted to investigate balance instability, using accelerometers during quiet stance with EO and EC in diabetic patients and healthy controls. The study found greater postural instability with higher acceleration in diabetic patients with peripheral neuropathy compared to controls and those without. Several studies also reported similar findings including greater center of pressure displacement, higher sway area in multidirections, and greater sway speed, indicating increased postural instability in diabetic patients with neuropathy., NIDDM patients recruited in our study have no reported history of neuropathy. This may explain why static balance was not significantly worse in diabetic compared to healthy control.
The strengths of our study were the used of comprehensive vestibular and balance test battery to quantify vestibular end organ function and functional mobility in NIDDM patients, whom were age matched with healthy controls. The small number of tested patients and controls in this study might cause increased in type II error. Another limitation is the exclusion of patients with hearing loss. There were evidence that DM could cause cochlear damage, resulting in hearing loss in diabetic patients. This is because of the close anatomical proximity and shared arterial blood supply between cochlear and vestibular peripheral system., With the mentioned exclusion criteria, we may potentially exclude those with significant vestibular dysfunction among diabetic patients. Therefore, it is suggested to include diabetic patients with hearing loss in future study. It is also suggested to include patients with neuropathy and to determine if vestibular system integrity would be different between patients with and without neuropathy.
| Conclusion|| |
Our findings showed that dynamic postural stability measured using TUG and FGA was significantly affected in NIDDM patients. This implies reduced functional mobility in them. Vestibular testing showed no significant difference between the two groups, suggesting normal vestibular function. Our study did not find any significant abnormal vestibular function in NIDDM patients as reported by previous authors. Further research studies are advocated.
The authors would like to thank dieticians in Dietetic Clinic, Klinik Warga Hospital, and Counselor Tuanku Muhriz, Pusat Perubatan Universiti Kebangsaan Malaysia (HCTM, PPUKM), for their assistance in the diabetic patients' recruitment. The study was conducted under the Universiti Kebangsaan Malaysia (UKM) Industri-2013-015 research grant support. The authors would like to thank SurgiPro Sdn Bhd for the in-kind contribution of the ICS Impulse GN Otometric. We would like to thank the Endowment from the Oticon Foundation Grant for the Eclipse EP25 Interacoustics. The authors gratefully acknowledge and thank Mr Galvin Teh from SurgiPro Sdn. Bhd. for his technical assistance and support on Brüel and Kjaer (Naerum, Denmark) mini-shaker 4810.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3]