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. Author manuscript; available in PMC: 2018 Dec 1.
Published in final edited form as: Int J Neurosci. 2017 Apr 25;127(12):1065–1073. doi: 10.1080/00207454.2017.1317249

Postural sway in individuals with type 2 diabetes and concurrent benign paroxysmal positional vertigo

Linda D’Silva 1,1, Patricia M Kluding 2, Susan L Whitney 3, Hongying Dai 4, Marcio Santos 5
PMCID: PMC5857488  NIHMSID: NIHMS949568  PMID: 28385058

Abstract

Background and Purpose

Diabetes has been shown to affect the peripheral vestibular end organs and is associated with an increase in the frequency of benign paroxysmal positional vertigo (BPPV). People with diabetes have higher postural sway; however, the impact of symptomatic BPPV on postural sway in individuals with diabetes is unclear. The purpose of this cross-sectional study was to examine postural sway in people with type 2 diabetes who have symptomatic, untreated BPPV (BPPVDM).

Methods

Fifty-two participants (mean age 56.9 ± 5.6 years) were enrolled: controls (n=14), diabetes (n=14), BPPV only (n=13) and BPPVDM (n=11). An inertial motion sensor was used to detect pelvic acceleration across five standing conditions with eyes open/closed on firm/foam surfaces. Range of acceleration (cm/s2), peak velocity (cm/s), and variability of sway (RMS) in the anterior-posterior (AP) and medial-lateral (ML) directions were used to compare postural sway between groups across conditions.

Results

Participants with BPPVDM had higher ranges of acceleration in the AP (p=0.02) and ML (p=0.02) directions, as well as higher peak velocity (p<0.001) and RMS values (p=0.006) in the AP direction compared to the control and diabetes groups. Standing on foam with eyes closed and tandem stance were challenging conditions for people with BPPVDM.

Conclusion

Clinicians may consider using standing on foam with eyes closed and tandem standing with eyes open to assess postural control in people with BPPVDM to identify postural instability.

Keywords: Postural sway, Type 2 diabetes, symptomatic, benign paroxysmal positional vertigo, accelerometry

Graphical Abstract

Range of acceleration and peak velocity were higher in the BPPVDM group in conditions 4 and 5 compared to controls and people with type 2 diabetes only. Additionally, peak velocity was higher in condition 2 compared to controls, people with type 2 diabetes and people with BPPV. BPPV-benign paroxysmal positional vertigo, DM-type 2 diabetes

graphic file with name nihms949568u1.jpg

Introduction

In people with type 2 diabetes, complications such as peripheral neuropathy and retinopathy contribute to increased postural sway and falls [1, 2]. Along with the somatosensory and visual systems, the vestibular system plays an important role in maintaining balance in static and dynamic conditions [3], and there is substantial evidence of reduced central and peripheral vestibular function in people with type 1 and type 2 diabetes [4, 5, 6]. In an epidemiological study, Agrawal et al. reported that vestibular dysfunction was 70% higher in people who had diabetes [7]; and people with diabetes, vestibular dysfunction and complaints of dizziness had twice the risk of falls [8].

One particular peripheral vestibular disorder, benign paroxysmal positional vertigo (BPPV), has been seen in higher frequency in people with diabetes [9, 10]. Cohen et al. reported that 14% of their subjects with BPPV had a history of diabetes [9]; while D’Silva et al. noted that BPPV was seen in 46% of individuals who had type 2 diabetes compared to 37% without diabetes [10]. In addition, the presence of comorbidities like diabetes and hypertension are linked to the increased recurrence rate of BPPV [11]. In BPPV, calcium carbonate crystals in the otolith organs of the inner ear are displaced into the semicircular canals [12]. The cause of this displacement has been postulated to be due to underlying degeneration of the macula of the otolith organs [12]. Diabetes, by increasing metabolic stress, has been shown to contribute to the degeneration of the otolith organs [6, 13, 14]. In fact, otolith dysfunction has been shown in people with diabetes, particularly in those with prolonged duration of diabetes and in those with poor glycemic control [13]. BPPV causes transient vertigo that is provoked by change in head position, and is associated with loss of balance and frequent falls [12].

People with symptomatic BPPV have higher postural sway compared to healthy controls, particularly in conditions with altered proprioception and vision [15]. Kinetic analysis of posture has been traditionally performed in single or double stance on a force platform while the different sensory systems (visual, vestibular and somatosensory) are perturbed [16, 17]. In people with BPPV, range and velocity of postural sway have been reported to be higher while standing on a foam pad with eyes closed [15]. Measures of postural sway decreased after treatment of the BPPV, showing that both range and velocity of sway are sensitive to dysfunction due to BPPV as well as to change with treatment [15]. Likewise, in people with diabetes and diabetic peripheral neuropathy (DPN), increased range and velocity of sway in the anterior-posterior and medial-lateral directions have been reported when compared to healthy controls, particularly with eyes closed [18, 19].

More recently, studies have used an accelerometer positioned near the center of mass, to measure postural sway quantitatively [20, 21]. Accelerometry has high validity and reliability when compared to center of pressure measures, using force platforms [22] and can discriminate between various test conditions, as the complexity of the task increases [21]. One 30-second trial of accelerometry has been shown to be as useful as three trials, to capture postural sway [22]. Time sensitive accelerometry measures that have been used to characterize postural sway include range of acceleration, root mean square of acceleration (RMS) and peak velocity [22, 23, 24]. Previous studies have shown that sway measures of RMS and peak velocity are stable with low variability in healthy controls [25].

The primary purpose of this study was to examine the impact of symptomatic posterior canal BPPV canalithiasis on postural sway in people with type 2 diabetes (BPPVDM). We used an accelerometer to assess postural sway in different visual and standing support conditions, which would challenge the vestibular system. We hypothesized that due to the combined effect of BPPV and DM, people with BPPVDM would have higher sway values compared to people with BPPV only, type 2 diabetes only and healthy controls. Our second aim was to identify which specific conditions of postural stability would be more challenging for people with BPPVDM. We hypothesized that people with BPPVDM would have greater difficulty maintaining a stable position in conditions with reduced visual and somatosensory information. Results of this study will be important to help clinicians understand the impact of a common comorbidity, diabetes, on postural stability in people with diabetes and concurrent BPPV.

1. Methods

1.1. Study Design

This was a cross-sectional study conducted at a university neuro-otology clinic. Participants were recruited from the neuro-otology clinic, internal medicine clinics, and through two university participant registries. The research protocol was approved by the institutional review board at the University of Kansas Medical Center. All participants signed the institutionally approved written informed consent prior to participation in the study.

1.2. Participants

Subjects who were between 40 to 65 years of age were recruited and allocated to one of four groups: healthy controls, people with type 2 diabetes without vestibular problems (diabetes), people with posterior canal BPPV canalithiasis without diabetes (BPPV), and those with both type 2 diabetes and BPPV (BPPVDM). People with BPPV and BPPVDM were diagnosed with unilateral posterior canal BPPV canalithiasis using videonystagmography. The presence of torsional up beating nystagmus in the Dix-Hallpike position, which had a brief latency, nystagmus lasting less than 60 seconds, with associated complaints of vertigo, was confirmed [12]. Participants with BPPV were untreated (i.e. symptomatic) when postural testing was conducted.

The presence or absence of diabetes was confirmed through a review of the individual’s electronic health records. To characterize the extent of diabetes control, glycated hemoglobin (HbA1c) information was collected via a disposable finger stick testing kit (Metrika A1cNow+ Bayer, Tarrytown NY). Glycated hemoglobin identifies average plasma glucose concentration based on the amount of glucose attached to hemoglobin, providing a useful long-term measure of blood glucose control. All participants were screened for the presence of sensory impairment using the Michigan Neuropathy Screening Instrument (MNSI). Participants were classified as having diabetic peripheral neuropathy (DPN) if their physical exam score was ≥ 2.0 (sensitivity of 65%, specificity of 83%) [26]. Participants with type 2 diabetes did not have any past medical diagnosis of a vestibular condition, identified in their health record and had no complaints of dizziness during the initial interview. The control group did not have a medical history of vestibular disease or diabetes on self-report.

Participants in all groups were excluded if they had (1) a history of neurological disease, (2) a history of Meniere’s disease, (3) received chemotherapy or ototoxic medications, (4) BMI > 45 kg/m2, (5) musculoskeletal conditions that would impair balance or (6) dependent on an assistive device for ambulation.

1.3. Materials and Procedure

Pelvic accelerations were measured using an inertial motion sensor (IMU; Xsens North America, USA; size 5.25 × 3.75 × 2 cm). The sensor was placed on the third vertebra of the lumbar spine and held in place using an elastic belt provided by the company (Figure 1).

Figure 1.

Figure 1

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The 5 experimental conditions used to examine postural sway. The inertial sensor was positioned at L3 spine level, displayed in the inset picture.

During a single testing session, participants were assessed in quiet standing for 30 seconds. Conditions tested were, Condition 1: standing on a firm surface with feet together, eyes open. Condition 2: Standing on a firm surface with feet together, eyes closed. Condition 3: Standing on a foam pad (Alimed balance pad elite™) with feet together and eyes open. Condition 4: standing on a foam pad with feet together, eyes closed. Condition 5: Tandem standing with eyes open on a firm surface. One trial was performed for each condition and all conditions were performed in the same order for all participants.

2. Data Processing

Data was acquired using the MT Manager software (Xsens North America Inc., Culver City, CA, USA) at a sampling frequency of 120 Hz. The three-axial (X, Y, and Z) acceleration data was recorded during the 30 seconds of data collection. The accelerations in Y and Z directions, corresponding to medial-lateral (ML) and anterior-posterior (AP) directions respectively, were used to calculate the variables that represented postural sway. The data was filtered with Butterworth 2nd order low-pass filter at 20 Hz and corrected for offset.

The following variables were calculated and used for analysis: (1) Range (cm/s2) – the peak-to-peak amplitude of acceleration, in AP (Range-AP) and ML directions (Range –ML), (2) peak velocity (cm/s) in AP (PV-AP) and ML (PV-ML) directions, velocity was calculated by integrating the acceleration, (3) root mean square (RMS) – the dispersion of the acceleration traces in AP (RMS-AP) and ML (RMS-ML) directions. All variables were calculated using customized Matlab code (Matlab R2015b, Mathworks Inc., Natick, MA, USA).

3. Statistical Analysis

Determination of sample size was made retrospectively based on a medium effect size seen when healthy controls were compared to people with posterior canal BPPV canalithiasis when standing on foam with eyes closed [15, 27]. Because of diabetes-related weakness and sensory deficits, we anticipated a medium effect size when comparing people with BPPVDM to healthy controls in that testing condition. Based on an effect size of 0.5, we needed a sample size of 10 per group, to provide 80% power.

Descriptive statistics (mean, standard deviation, %) are used to present subject demographics in each group. After data were analyzed for skewness and normality, group differences in subject demographics were tested using ANOVA and Tukey’s HSD for variables that were significantly different between groups. Range-AP, range-ML, PV-AP, PV-ML, RMS-AP and RMS-ML were examined using a general linear mixed model method with sex, BMI and DPN as covariates. Main effects are reported as F-values, and p-values. Effect size is reported as partial eta squared, where 0.01 represents a small effect size, 0.06 a medium effect size and 0.14 a large effect size. For a significant model, post hoc comparisons were conducted. In those trials in which participants were unable to complete the test, we used an intention to treat model, and values were assigned based on the group mean ± 2SD. Pearson correlations were used to examine the relationship between glycemic control and postural sway variables. Statistical analysis was performed using SPSS 20.0 (SPSS, Inc., Chicago, IL) with significance level set at 0.05.

4. Results

We screened 151 people and enrolled 52 in the four participant groups: 1) controls (n=14), 2) type 2 diabetes (n=14), 3) BPPV (n=13), and 4) BPPVDM (n=11).

4.1. Descriptive statistics

Participant characteristics are summarized in Table 1. Participants wore corrective glasses as needed while participating in the study. Since BMI was significantly higher in both groups with diabetes, and gender and neuropathy status varied between groups, repeated measures analyses were conducted with BMI, gender and DPN as covariates. No main effects were seen for gender and BMI in any variable, hence, results shown below address the impact of DPN on postural sway. One participant in the BPPVDM group could not stand on foam, eyes closed or tandem stance, while another participant was unable to complete tandem stance, due to loss of balance.

Table 1.

Baseline Participant Characteristics by Group

Controls (n-14) Type 2 DM (n=14) BPPV (n=13) BPPVDM (n=11) p-value
Age (years) 58.07 (4.9) 57.4 (5.5) 54.5 (6.0) 57.6 (5.7) p= 0.34
Gender (M/F) 3/11 2/12 2/11 3/8
HbA1c (%) 5.4 (0.4) 7.8 (1.9)§ 5.6 (0.4) 6.9 (1.6)§ p< 0.001
BMI (kg/m2) 27.2 (6.3) 34.0 (5.1)† 28.2 (6.5) 36.3 (4.2)† p<0.001
95% CI (23.6–30.86) (30.9–36.9) (24.2–32.1) (33.5–39.2)
Normal weight 5 0 3 0
Overweight 6 4 6 0
Class I obesity 0 5 2 4
Class II obesity 3 3 1 4
Class III obesity 0 2 1 3
Years with DM 10.4 ± 8.7 11.0 ± 12.6
DPN 0 57% (n=8) 0 36% (n=4)
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Post hoc comparisons show §HbA1c and †BMI were significantly higher in the type 2 DM and BPPVDM groups compared to controls and BPPV groups.

Values are presented as mean ± SD or frequency. DM- diabetes mellitus, BPPV- benign paroxysmal positional vertigo, BPPVDM- diabetes and concurrent BPPV, DPN-diabetic peripheral neuropathy, BMI-body mass index, HbA1c- glycosylated hemoglobin. BMI between 18.5–24.9=normal weight, BMI 25.0–29.9= overweight, BMI 30.0–34.9= class I obesity, BMI 35.0–39.9= class II obesity, BMI ≥ 40.0= class III obesity

4.2. Postural Sway variables

Range of acceleration

For range-AP, results showed a main effect for group (F1, 52: 5.49, p=0.003, partial eta squared=0.27), condition (F 1, 52: 34.6, p<0.001, partial eta squared=0.42), interaction between group and condition (F 1, 52: 2.6, p=0.004, partial eta squared=0.15), and a main effect of DPN (F 1,52: 9.5, p=0.003, partial eta squared=0.18). The BPPVDM group had higher range-AP on foam, eyes closed (1.08 ± 0.1 cm/s2) compared to the control group (0.8 ± 0.1cm/s2, p=0.08) and the diabetes group (0.7 ± 0.1 cm/s2, p=0.01). In tandem stance, the BPPVDM group had higher range-AP (0.8 ± 0.1 cm/s2) compared to controls (0.5 ± 0.1 cm/s2, p=0.03) and the diabetes group (0.4 ±0.1cm/s2, p=0.003) (Figure 2). No differences were noted in range-AP between the BPPV and BPPVDM groups in any condition. People with DPN had increased AP range of sway when standing on the foam pad with eyes closed (p=0.003), and in tandem standing (p=0.001) compared to people without DPN.

Figure 2.

Figure 2

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Mean and standard error of range in the anteroposterior (AP) and mediolateral (ML) directions for the four groups across the five testing conditions. a and b indicate the significant difference between the BPPVDM and BPPV groups compared to the control and diabetes groups respectively.

Range-ML showed a main effect for group (F1, 52: 6.1, p=0.001, partial eta squared=0.29), condition (F 1, 52: 3.65, p=0.007, partial eta squared=0.08), and DPN (F1,52: 7.1, p=0.01, partial eta squared=0.14), there was no interaction between group and condition (F 1, 52: 1.5, p=0.05, partial eta squared=0.11). The BPPVDM group had higher range-ML on foam with eyes closed (1.39 ± 0.1 cm/s2) compared to controls (1.1 ± 0.1cm/s2, p=0.03) and the diabetes groups (1.0 ± 0.1cm/s2, p=0.01). In tandem stance, the BPPVDM group had higher range-ML (0.9 ± 0.1 cm/s2) compared to controls (0.6 ± 0.1 cm/s2, p=0.05) and the diabetes group (0.5 ± 0.1 cm/s2, p=0.004) (Figure 2). No differences were noted in range-ML between the BPPV and BPPVDM groups in any condition. People with DPN had higher range-ML when standing on foam with eyes closed (p=0.01) and in tandem standing (p<0.001), compared to those without DPN.

Peak velocity

Peak velocity-AP showed a main effect for group (F1, 52: 8.3, p<0.001, partial eta squared=0.36), condition (F1, 52:18.11, p<0.001, partial eta squared=0.5), with no interaction noted between group and condition (F1, 52: 1.8, p=0.1, partial eta squared=0.1), interaction was noted between DPN and condition (F1,52:2.49, p=0.04, partial eta squared=0.05). Peak velocity AP was higher in the BPPVDM group (0.04 ± 0.001 cm/s) compared to the control (0.01 ± 0.001 cm/s, p<0.001), diabetes (0.02 ± 0.002 cm/s, p=0.001) and BPPV groups (0.02 ±0.004 cm/s, p=0.04) when standing on a firm surface with eyes closed. Higher PV-AP was seen in the BPPVDM group (0.04 ± 0.004 cm/s) when standing on foam with eyes closed compared to controls (0.03 ±0.003 cm/s, p=0.05) and the diabetes groups (0.03 ± 0.003, p=0.004). Higher PV-AP was present in the BPPVDM group in tandem stance (0.04 ± 0.004 cm/s) compared to controls (0.02 ± 0.004, p=0.04) and the diabetes group (0.02 ± 0.004, p<0.001) (Figure 3). No differences were noted in PV-AP between the BPPV and BPPVDM groups when standing on foam with eyes closed or in tandem standing with eyes open. People with DPN had higher PV-AP when standing on foam with eyes closed (p= 0.001) and in tandem standing (p<0.001) compared to people without DPN.

Figure 3.

Figure 3

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Mean and standard error of peak velocity in the anteroposterior (AP) and mediolateral (ML) direction for the four groups across the five testing conditions. a and b indicate the significant differences between the BPPVDM and BPPV groups and the control and diabetes groups respectively. c indicates the significant difference between the BPPVDM group and the 3 other groups.

Peak velocity-ML had a main effect for condition (F1, 52: 10.5, p<0.001, partial eta squared=0.18). The main effect for group (F1, 52: 1.9, p=0.1, partial eta squared=0.11), and interaction (F1, 52: 1.2, p=0.3, partial eta squared=0.07) was not significant. There was interaction between condition and DPN (F1,52: 2.4, p=0.05, partial eta squared= 0.05). Subsequent analysis showed that higher PV-ML was seen in the BPPVDM group (0.14 ± 0.02 cm/s) when standing on foam with eyes closed when compared to controls (0.05 ± 0.02 cm/s, p=0.0007), diabetes (0.05 ± 0.02 cm/s, p<0.001) and BPPV groups (0.07 ± 0.02 cm/s, p=0.01). People with DPN had higher PV-ML in tandem standing (p=0.001) compared to people without DPN.

Root Mean Square

RMS-AP showed a main effect for condition (F 1, 52: 14.73, p<0.001, partial eta squared=0.24) and interaction between group and condition (F1, 52: 2.43, p=0.006, partial eta squared=0.13). There was no main effect of group (F 1, 52: 1.32, p=0.28, partial eta squared=0.08), however, a main effect of DPN (F 1,52: 7.09, p=0.01, partial eta squared=0.13) was seen. The BPPVDM group had higher RMS-AP (0.3 ± 0.03) in tandem stance compared to controls (0.15 ± 0.03, p=0.024), and diabetes groups (0.15 ± 0.03, p=0.02). People with DPN had increased RMS-AP in tandem standing (p=0.04) compared to those without DPN. Highest RMS-AP was seen in the BPPV group when standing on foam with eyes closed (Figure 4).

Figure 4.

Figure 4

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Mean and standard error of RMS of acceleration in the anteroposterior (AP) and mediolateral (ML) directions for the four groups across the five testing conditions. Based on condition, a indicates the difference between the BPPVDM and control and diabetes groups, and d indicates the difference between the BPPV groups and the three other groups.

RMS-ML showed a main effect for condition (F 1, 52: 37.4, p<0.001, partial eta squared=0.44). There was no interaction between group and condition (F 1, 52: 0.49, p= 0.92, partial eta squared=0.03), and there was no main effect for group (F 1, 52: 1.2, p=0.26, partial eta squared=0.08) or DPN (F1,52: 0.99, p=0.17, partial eta squared=0.02). Higher RMS-ML in all groups was seen when standing on foam with eyes closed.

In people with a history of DM, both DM only and BPPVDM, significant correlations were seen between HbA1c and range-AP (r=0.47) and RMS-AP (r=0.52) when standing on foam with eyes open, and range-AP (r=0.43) and RMS-AP (r=0.47) in tandem standing.

5. Discussion

The main findings of our study partially supported our primary hypothesis that people with type 2 diabetes and concurrent BPPV would exhibit increased postural sway compared to people with BPPV only, diabetes only and healthy controls, suggestive of decreased postural stability. Our second aim was to identify the conditions that would be challenging for people with BPPVDM. Our results showed that standing on a complaint surface without visual input and tandem stance were challenging positions for people with BPPVDM but they were equally challenging for people with BPPV only. The only position that was significantly more challenging for people with BPPVDM was standing on a firm surface with eyes closed.

The vestibular system, along with the visual and somatosensory systems provides information about the position and motion of the body with respect to earth’s vertical. In normal conditions, information from all sensory systems complement each other, however, if one of the sensory inputs is unavailable or deprived, it is critical for the central nervous system be able to extract sensory information from the other available sensory systems (sensory reweighting) to maintain postural stability and avoid a fall [28]. Results of our study suggest that the presence of BPPV may modify sway during stance. These results are similar to the findings of previous studies using static posturography, which have shown higher range and velocity of sway in people with posterior canal BPPV when standing on foam with eyes closed [15, 27].

When we examined participants in tandem stance, we found that higher sway (range-AP, range-ML, and PV-AP, RMS-AP) was seen in the BPPVDM group compared to controls and those with type 2 DM. In tandem stance where the support surface is reduced, hip strategy is inherently utilized to control the center of mass, however, people with vestibular dysfunction have difficulty utilizing hip strategy [29]. Additionally, somatosensory feedback from the feet is essential in tandem stance, due to the smaller base of support. Results of this study showed that people with BPPVDM, particularly those with DPN had increased sway compared to those without DPN. Like the BPPVDM group, the people with BPPV only had higher sway in tandem stance, however, sway in the BPPV group was not higher than the control and DM groups. This study shows that in tandem standing, people with BPPVDM and coexisting DPN have decreased postural stability, which could increase their risk for falling. Tandem standing could be used as a quick and effective assessment tool in the clinic setting to identify balance deficits in people 65 years of age and younger with vestibular and somatosensory deficits.

Recent studies have shown that otolith organ function is impaired in people with type 2 diabetes, particularly in those with a longer duration of diabetes [6, 13]. Animal studies have shown morphological changes in the saccule of rats in experimentally induced diabetes due to metabolic stress [14]. The otolith organs provide the primary vestibular contribution to postural control [30]; and damage to the otolith organs has been shown to affect postural control [31]. Because of the effect of diabetes on the saccule, we had hypothesized that people with BPPVDM would have higher sway compared to people with BPPV only, DM only and healthy controls. However, the only variable in which people with BPPVDM had increased postural sway compared to the three other groups was PV-AP when standing on a firm surface with eyes closed. We found no differences between people with BPPVDM and those with BPPV only when standing on foam with eyes closed or in tandem stance, the two most difficult conditions to perform. The findings may have been different if older subjects with a longer duration of diabetes had been recruited. The present study was not designed to examine the impact of diabetes directly on the vestibular system, but it can stimulate future studies to investigate the relationship between postural sway and direct measures of vestibular function.

One observation of this study was that significant differences between groups were seen more frequently in the AP (range, peak velocity and RMS) than in the ML direction. One possible explanation for this finding is that in bipedal stance, there is more range of motion available in the ankle, knee and hip joints, which can be utilized to maintain balance, using the ankle, hip and suspensory strategies [17]. Additionally, in people with BPPV, higher AP sway values have been observed when standing on a foam pad and with eyes closed [15, 27]. The significant differences between groups in the AP direction may represent the different strategies used by participants to control balance in the sagittal plane. Our study found that the ML sway values also tended to be higher for all groups of participants when standing on foam and in the eyes closed conditions, although differences between groups were not as frequent, hence, we suggest that clinicians observe sway in both AP and ML directions during balance testing.

We found no differences in any measure of postural sway in people with type 2 diabetes compared to controls. Previous studies using center of pressure displacement calculated from force platforms have shown that people with type 2 diabetes, particularly those with diabetic peripheral neuropathy (DPN), have greater range and velocity of sway compared to age matched controls, when standing on a firm surface with and without visual input [18]. This difference may be because our subjects were younger, with well controlled diabetes where the average HbA1c was 7.8 ± 1.9 in people with diabetes and 6.9 ± 1.6 in those with BPPVDM. We did find significant correlations between glycemic control and postural sway, which was seen in tandem standing. Future studies examining glycemic control, duration of diabetes, severity of neuropathy, and their relationship to postural instability in people with BPPVDM are necessary to identify fall risk.

Ultimately, the significance of finding increased postural sway in people with BPPVDM is related to its potential association with falls. O’Sullivan et al. [24] have shown higher RMS sway values using accelerometry in older adults who walked slower on the Timed-up-and-go (TUG) test, and slower TUG scores are strongly related to fall risk [32]. This study showed differences in postural sway between people with BPPVDM and all other groups in different conditions, however, we did not look at fall history in this study, hence, we cannot determine if the difference in sway is meaningful related to risk of falling. Postural stability is compromised in people with BPPV with and without diabetes, especially when somatosensory and visual feedback are deprived, and deteriorates further in the presence of diabetic peripheral neuropathy. Hence, certain daily activities like walking in the yard without adequate lighting could increase fall risk. Fortunately, BPPV can be treated effectively using the canalith repositioning maneuver, and has a treatment efficacy rate of 85% with a single treatment maneuver [33]. Given the higher frequency of BPPV in persons with diabetes, the higher risk for falls in persons with diabetes [34, 35], plus more severe injuries after a fall [36, 37], it is essential to diagnose and treat BPPV promptly to avoid falls and their ensuing complications.

6. Conclusion

People with symptomatic BPPV both with and without type 2 diabetes have higher postural sway when standing on a compliant surface with eyes closed and in tandem standing compared to people with diabetes only and healthy controls. The presence of diabetic peripheral neuropathy can further decrease postural stability. In people with BPPV, diabetes and peripheral neuropathy, tandem standing may be an easy test to perform in the clinical setting to detect postural instability.

Acknowledgments

This work was supported by an institutional grant T32HD057850 from the Eunice Kennedy Shriver National Institute of Child Health & Human Development. The Kansas Partners in Progress grant, which is sponsored by the Kansas Physical Therapy Association. REDCap at the University of Kansas Medical Center is supported by CTSA grant (CTSA Award # UL1TR000001) from NCRR and NCATS awarded to the University of Kansas Medical Center. The funding source had no involvement in the study process or publication decision.

Footnotes

Declaration of Interest:

The authors declare no conflict of interest.

Contributor Information

Linda D’Silva, Department of Physical Therapy and Rehabilitation Science, University of Kansas Medical Center, 3901 Rainbow Blvd, Kansas City, KS 66160. USA.

Patricia M. Kluding, Associate Professor and Interim Chair of the Department of Physical Therapy and Rehabilitation Science, University of Kansas Medical Center, Kansas City, KS 66160, USA.

Susan L. Whitney, University of Pittsburgh, School of Health and Rehabilitation Sciences, Pittsburgh, PA 15260, USA; Secondary affiliation, Rehabilitation Research Chair, Department of Rehabilitation Sciences, King Saud University, Riyadh, Saudi Arabia

Hongying Dai, Health Services and Outcomes Research, Children’s Mercy Hospital, Kansas City, MO 64108, USA.

Marcio Santos, Department of Physical Therapy and Rehabilitation Science, University of Kansas Medical Center, Kansas City, KS 66160, USA.

References

  • 1.Brown SJ, Handsaker JC, Bowling FL, Boulton AJ, Reeves ND. Diabetic peripheral neuropathy compromises balance during daily activities. Diabetes Care. 2015;38:1116–22. doi: 10.2337/dc14-1982. Epub 2015/03/15. [DOI] [PubMed] [Google Scholar]
  • 2.Ivers RQ, Cumming RG, Mitchell P, Peduto AJ. Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. 2001;24:1198–203. doi: 10.2337/diacare.24.7.1198. Epub 2001/06/26. [DOI] [PubMed] [Google Scholar]
  • 3.Mirka A, Black FO. Clinical application of dynamic posturography for evaluating sensory integration and vestibular dysfunction. Neurol Clin. 1990;8:351–9. Epub 1990/05/01. [PubMed] [Google Scholar]
  • 4.D’Silva LJ, Lin J, Staecker H, Whitney SL, Kluding PM. Impact of Diabetic Complications on Balance and Falls: Contribution of the Vestibular System. Phys Ther. 2015 doi: 10.2522/ptj.20140604. Epub 2015/08/08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Gawron W, Pospiech L, Orendorz-Fraczkowska K, Noczynska A. Are there any disturbances in vestibular organ of children and young adults with Type I diabetes? Diabetologia. 2002;45:728–34. doi: 10.1007/s00125-002-0813-x. Epub 2002/07/11. [DOI] [PubMed] [Google Scholar]
  • 6.Ward BK, Wenzel A, Kalyani RR, Agrawal Y, Feng AL, Polydefkis M, Ying HS, Schubert MC, Zuniga MG, Della Santina CC, Carey JP. Characterization of Vestibulopathy in Individuals with Type 2 Diabetes Mellitus. Otolaryngol Head Neck Surg. 2015;153:112–8. doi: 10.1177/0194599815576717. Epub 2015/04/02. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Agrawal Y, Carey JP, Della Santina CC, Schubert MC, Minor LB. Disorders of balance and vestibular function in US adults: data from the National Health and Nutrition Examination Survey, 2001–2004. Arch Intern Med. 2009;169:938–44. doi: 10.1001/archinternmed.2009.66. Epub 2009/05/27. [DOI] [PubMed] [Google Scholar]
  • 8.Agrawal Y, Carey JP, Della Santina CC, Schubert MC, Minor LB. Diabetes, vestibular dysfunction, and falls: analyses from the National Health and Nutrition Examination Survey. Otology & neurotology: official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology. 2010;31:1445–50. doi: 10.1097/MAO.0b013e3181f2f035. Epub 2010/09/22. [DOI] [PubMed] [Google Scholar]
  • 9.Cohen HS, Kimball KT, Stewart MG. Benign paroxysmal positional vertigo and comorbid conditions. ORL J Otorhinolaryngol Relat Spec. 2004;66:11–5. doi: 10.1159/000077227. Epub 2004/04/23. [DOI] [PubMed] [Google Scholar]
  • 10.D’Silva LJ, Staecker H, Lin J, Sykes KJ, Phadnis MA, McMahon TM, Connolly D, Sabus CH, Whitney SL, Kluding PM. Retrospective data suggests that the higher prevalence of benign paroxysmal positional vertigo in individuals with type 2 diabetes is mediated by hypertension. J Vestib Res. 2016;25:233–9. doi: 10.3233/VES-150563. Epub 2016/02/20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.De Stefano A, Dispenza F, Suarez H, Perez-Fernandez N, Manrique-Huarte R, Ban JH, Kim MB, Strupp M, Feil K, Oliveira CA, Sampaio AL, Araujo MF, Bahmad F, Jr, Gananca MM, Gananca FF, Dorigueto R, Lee H, Kulamarva G, Mathur N, Di Giovanni P, Petrucci AG, Staniscia T, Citraro L, Croce A. A multicenter observational study on the role of comorbidities in the recurrent episodes of benign paroxysmal positional vertigo. Auris Nasus Larynx. 2014;41:31–6. doi: 10.1016/j.anl.2013.07.007. Epub 2013/08/13. [DOI] [PubMed] [Google Scholar]
  • 12.Bhattacharyya N, Baugh RF, Orvidas L, Barrs D, Bronston LJ, Cass S, Chalian AA, Desmond AL, Earll JM, Fife TD, Fuller DC, Judge JO, Mann NR, Rosenfeld RM, Schuring LT, Steiner RW, Whitney SL, Haidari J. Clinical practice guideline: benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg. 2008;139:S47–81. doi: 10.1016/j.otohns.2008.08.022. Epub 2008/12/05. [DOI] [PubMed] [Google Scholar]
  • 13.Konukseven O, Polat SB, Karahan S, Konukseven E, Ersoy R, Cakir B, Kutluhan A, Aksoy S. Electrophysiologic vestibular evaluation in type 2 diabetic and prediabetic patients: Air conduction ocular and cervical vestibular evoked myogenic potentials. Int J Audiol. 2014:1–8. doi: 10.3109/14992027.2014.971887. Epub 2014/12/23. [DOI] [PubMed] [Google Scholar]
  • 14.Myers SF, Ross MD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. II. Connective tissue and neuroepithelial pathology. Acta Otolaryngol. 1987;104:40–9. doi: 10.3109/00016488709109045. Epub 1987/07/01. [DOI] [PubMed] [Google Scholar]
  • 15.Celebisoy N, Bayam E, Gulec F, Kose T, Akyurekli O. Balance in posterior and horizontal canal type benign paroxysmal positional vertigo before and after canalith repositioning maneuvers. Gait Posture. 2009;29:520–3. doi: 10.1016/j.gaitpost.2008.12.002. Epub 2009/01/14. [DOI] [PubMed] [Google Scholar]
  • 16.Di Nardo W, Ghirlanda G, Cercone S, Pitocco D, Soponara C, Cosenza A, Paludetti G, Di Leo MA, Galli I. The use of dynamic posturography to detect neurosensorial disorder in IDDM without clinical neuropathy. J Diabetes Complications. 1999;13:79–85. doi: 10.1016/s1056-8727(99)00032-x. Epub 1999/08/04. [DOI] [PubMed] [Google Scholar]
  • 17.McCollum G, Shupert CL, Nashner LM. Organizing sensory information for postural control in altered sensory environments. J Theor Biol. 1996;180:257–70. doi: 10.1006/jtbi.1996.0101. Epub 1996/06/07. [DOI] [PubMed] [Google Scholar]
  • 18.Boucher P, Teasdale N, Courtemanche R, Bard C, Fleury M. Postural stability in diabetic polyneuropathy. Diabetes Care. 1995;18:638–45. doi: 10.2337/diacare.18.5.638. Epub 1995/05/01. [DOI] [PubMed] [Google Scholar]
  • 19.Corriveau H, Prince F, Hebert R, Raiche M, Tessier D, Maheux P, Ardilouze JL. Evaluation of postural stability in elderly with diabetic neuropathy. Diabetes Care. 2000;23:1187–91. doi: 10.2337/diacare.23.8.1187. Epub 2000/08/11. [DOI] [PubMed] [Google Scholar]
  • 20.Marchetti GF, Bellanca J, Whitney SL, Lin JC, Musolino MC, Furman GR, Redfern MS. The development of an accelerometer-based measure of human upright static anterior- posterior postural sway under various sensory conditions: Test-retest reliability, scoring and preliminary validity of the Balance Accelerometry Measure (BAM) J Vestib Res. 2013;23:227–35. doi: 10.3233/VES-130490. Epub 2013/11/29. [DOI] [PubMed] [Google Scholar]
  • 21.Moe-Nilssen R, Helbostad JL. Trunk accelerometry as a measure of balance control during quiet standing. Gait Posture. 2002;16:60–8. doi: 10.1016/s0966-6362(01)00200-4. Epub 2002/07/20. [DOI] [PubMed] [Google Scholar]
  • 22.Whitney SL, Roche JL, Marchetti GF, Lin CC, Steed DP, Furman GR, Musolino MC, Redfern MS. A comparison of accelerometry and center of pressure measures during computerized dynamic posturography: a measure of balance. Gait Posture. 2011;33:594–9. doi: 10.1016/j.gaitpost.2011.01.015. Epub 2011/02/22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Mancini M, Salarian A, Carlson-Kuhta P, Zampieri C, King L, Chiari L, Horak FB. ISway: a sensitive, valid and reliable measure of postural control. J Neuroeng Rehabil. 2012;9:59. doi: 10.1186/1743-0003-9-59. Epub 2012/08/24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.O’Sullivan M, Blake C, Cunningham C, Boyle G, Finucane C. Correlation of accelerometry with clinical balance tests in older fallers and non-fallers. Age Ageing. 2009;38:308–13. doi: 10.1093/ageing/afp009. Epub 2009/03/03. [DOI] [PubMed] [Google Scholar]
  • 25.Mancini M, Carlson-Kuhta P, Zampieri C, Nutt JG, Chiari L, Horak FB. Postural sway as a marker of progression in Parkinson’s disease: a pilot longitudinal study. Gait Posture. 2012;36:471–6. doi: 10.1016/j.gaitpost.2012.04.010. Epub 2012/07/04. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Moghtaderi A, Bakhshipour A, Rashidi H. Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg. 2006;108:477–81. doi: 10.1016/j.clineuro.2005.08.003. Epub 2005/09/10. [DOI] [PubMed] [Google Scholar]
  • 27.Chang WC, Hsu LC, Yang YR, Wang RY. Balance ability in patients with benign paroxysmal positional vertigo. Otolaryngol Head Neck Surg. 2006;135:534–40. doi: 10.1016/j.otohns.2005.10.001. Epub 2006/10/03. [DOI] [PubMed] [Google Scholar]
  • 28.Herdman SJ. Vestibular rehabilitation. Current opinion in neurology. 2013;26:96–101. doi: 10.1097/WCO.0b013e32835c5ec4. Epub 2012/12/18. [DOI] [PubMed] [Google Scholar]
  • 29.Herdman S. Vestibular Rehabilitation. 2. 2000. [Google Scholar]
  • 30.Akin FW, Murnane OD, Tampas JW, Clinard CG. The effect of age on the vestibular evoked myogenic potential and sternocleidomastoid muscle tonic electromyogram level. Ear Hear. 2011;32:617–22. doi: 10.1097/AUD.0b013e318213488e. Epub 2011/03/24. [DOI] [PubMed] [Google Scholar]
  • 31.McCaslin DL, Jacobson GP, Grantham SL, Piker EG, Verghese S. The influence of unilateral saccular impairment on functional balance performance and self-report dizziness. J Am Acad Audiol. 2011;22:542–9. doi: 10.3766/jaaa.22.8.6. quiz 60-1. Epub 2011/10/28. [DOI] [PubMed] [Google Scholar]
  • 32.Whitney SL, Marchetti GF, Schade A, Wrisley DM. The sensitivity and specificity of the Timed “Up & Go” and the Dynamic Gait Index for self-reported falls in persons with vestibular disorders. J Vestib Res. 2004;14:397–409. Epub 2004/12/16. [PubMed] [Google Scholar]
  • 33.Prokopakis E, Vlastos IM, Tsagournisakis M, Christodoulou P, Kawauchi H, Velegrakis G. Canalith repositioning procedures among 965 patients with benign paroxysmal positional vertigo. Audiol Neurootol. 2013;18:83–8. doi: 10.1159/000343579. Epub 2012/11/14. [DOI] [PubMed] [Google Scholar]
  • 34.Schwartz AV, Vittinghoff E, Sellmeyer DE, Feingold KR, de Rekeneire N, Strotmeyer ES, Shorr RI, Vinik AI, Odden MC, Park SW, Faulkner KA, Harris TB. Diabetes-related complications, glycemic control, and falls in older adults. Diabetes Care. 2008;31:391–6. doi: 10.2337/dc07-1152. Epub 2007/12/07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Chiles NS, Phillips CL, Volpato S, Bandinelli S, Ferrucci L, Guralnik JM, Patel KV. Diabetes, peripheral neuropathy, and lower-extremity function. J Diabetes Complications. 2014;28:91–5. doi: 10.1016/j.jdiacomp.2013.08.007. Epub 2013/10/15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TT, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV. Fracture risk in diabetic elderly men: the MrOS study. Diabetologia. 2014;57:2057–65. doi: 10.1007/s00125-014-3289-6. Epub 2014/06/09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165:1612–7. doi: 10.1001/archinte.165.14.1612. Epub 2005/07/27. [DOI] [PubMed] [Google Scholar]

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