Balance performance, falls-efficacy and social participation in patients with type 2 diabetes mellitus with and without vestibular dysfunction

Introduction

Inputs from three systems, including visual, proprioception and vestibular, play important roles in postural control, especially when performing dynamic tasks. The integration of these sensations regulates appropriate timed and scaled outputs to preserve the postural control (Mancini & Horak, 2010; Sibley et al., 2015). A greater number of impaired sensory systems is presented with different levels of difficulties related to balance and falls (Kraiwong et al., 2019). The impairment of sensory systems and lower balance performance in patients with T2DM are associated with microvascular complications. Neuropathy (DPN) is the most common complication that diminished the function of proprioception, presenting in 60–70% of chronic T2DM (Centers for Disease Control and Prevention., 2011; Purwanti & Novitasari, 2021). DPN alters movement as a result of the diminished perceptions of touch, temperature, and pain, and reduced proprioceptive inputs leading to difficulty in ambulation and falling (Brod et al., 2015). The DPN can develop into the foot ulcers without good management that can interfere the gait and increase fall (Rosyid, 2017). Another common complication of T2DM, the diabetic retinopathy (DR) which impacts the reduction in visual system, had also been reported to increase with age and brought a 25 times higher risk of losing vision compared with people without DM (Jenkins et al., 2015). These two common microvascular complications largely contributed to the elevated postural sway (Brod et al., 2015; Schwartz et al., 2008).

Along with the visual and somatosensory functions, the vestibular system also plays an important role in controlling balance especially when the head moved. Vestibular dysfunction (VD) has been recognized as an independent factor of falling. Diminished sensitivity of the vestibular system can alter perception regarding motion, equilibrium, and spatial orientation which is necessary to maintain stability (Goble et al., 2019). A survey in the US found a VD prevalence of 70% among participants with DM aged 40 years or older (Agrawal et al., 2009). The risk of falling increases two-fold in DM patients with VD who had long duration of DM (≥5 years) compared with the group without VD (Agrawal et al., 2010). Moreover, dizziness which is the most common symptom of VD was reported in 20–30% of the general population. Participants with symptomatic VD had dizziness symptoms and had 12 times increasing of falling (Agrawal et al., 2009).

Falls-efficacy (FE) is the self-perceived rating to perform activities of daily living without falling (Tinetti, Richman & Powell, 1990). This factor has been proposed to be a critical indicator of diabetes self-care and a risk factor for falls. Reduction of self-efficacy becomes self-blame, worse self-complaint, and criticisms from others that might further affect the quality of life (QoL). The low self-efficacy were prevalent among older adults, affecting 33 to 46% of older adult non-fallers and up to 85% of older adult fallers (Kumar et al., 2014).

The World Health Organization has declared social participation as a substantial component of active aging (WHO, 2002). Social participation is defined as the involvement in activities and interactions with other people in a social or community frame. Persons with DM reported higher probability of a lack of social involvement, but the contribution of disability related with DM to the social life has not been fully explored (Brinkhues et al., 2017; Weidt et al., 2014).

The aging process is a factor deteriorating the body function in elderly including balance control. A previous study reported that people with DM had poorer balance than without DM. Diminished balance performance is occurred in DM, even without sensory impairment (Kraiwong et al., 2019). The consequences of DPN and DR associated with T2DM on gait instability and falls are well documented. However, the information about VD effects is rather poorly recognized (Agrawal et al., 2010; D’Silva et al., 2016). The VD symptoms of dizziness and imbalance were considered to be the main predictors of falling in the elderly and might also decrease balance confidence. However, few studies had evaluated the FE associated with diminished balance and increased fear of falling (FoF) in patients with DM. A recent study reported that T2DM patients with VD had severe restrictions in social participation and also had movement difficulty due to the dizziness feeling (Komalasari et al., 2022). Another study showed that among 34 activities in the Vestibular Activities Participation (VAP) questionnaire, 10 activities were difficult to be carried out by VD patients (Alghwiri, Alghadir & Whitney, 2013). The inference of having VD on the factors associated with falls including balance performance, fall-efficacy, social participation and quality of life among individuals with T2DM needs more exploration. Therefore, this study aimed to compare balance performance, falls-efficacy, social participation and quality of life between individuals with T2DM with and without vestibular dysfunction.

Materials and Methods

This study was a cross-sectional, comparative research. It was conducted after the approval from the ethics committee of Mahidol University Institutional Review Board (MU-CIRB 2020/098.2004) and the Medical Faculty, Universitas Muhammadiyah Surakarta, Indonesia (No. 3009/B.1/KEPK-FKUMS/VII/2020).

Results

The participants consisted of 161 T2DM with VD and 161 T2DM without VD. As presented in Table 1, there were no significant differences between the groups for the personal characteristics.

The numbers of female participants were greater in both groups. The participants in both groups had the same average age and around half of them had hypertension. No differences about hypertension and normal tension between two groups. Likewise, around three-fourths of the participants in both groups suffered from T2DM between 5–10 years. Regarding the cut level of fasting period by the World Health Organization, most of them also had high fasting glycemic levels (>125 mg/dl) (WHO, 1999), especially in the group with VD which 72% were presented with high FGL levels. More participants had normal BMI; nevertheless, almost 50% of the participants were overweight in both groups. Approximately one-fifth of participants in both groups experienced a fall once in the past year.

The results of clinical examination are summarized in Table 2. There were no significant differences for pain, DPN, and cognitive function between T2DM with VD and without VD groups. The lower leg pain was on average five of 10 measured by NRS for both groups. The score and proportion of participants with DPN were not different between groups. The average score of visual acuity was different but there was no difference of the percentages of participants with low visual acuity between groups.

The time of 5XSST was significantly different (p <  0.001) between groups. The average score of Moca-Ina and the proportion of ones with cognitive impairment were not different between groups. Both groups had persons mostly with mild and some with moderate cognitive impairment.

As shown in Table 3, the static balance measured by total scores of mCTSIB test was significantly different between two groups (p < 0.001). The group with VD had lower static balance performance compared to those without VD. Likewise, conditions 2 (p = 0.02), 3 and 4 (p < 0.001) of mCTSIB were significantly different between groups. However, the time used in condition 1 of mCTSIB was not significantly different between groups (p = 0.357). For dynamic balance, the total scores of TUG (p = 0.001) and FGA (p = 0.01) were significantly different between groups. The total scores of FE measured by ABC-16-Ina were significantly different between two groups (p < 0.001). FE in T2DM without VD group was higher than in T2DM with the VD group.

There were significant differences for PSSS and LSA among groups, and the T2DM with VD group had lower social quality than T2DM without VD measured by LSA and PSSS. The number of participants with severe restriction was higher in T2DM with VD group than without VD. The total scores and all domains of WHOQoL were also different between groups (p < 0.001). The T2DM with VD had lower QoL compared with T2DM without VD.

Figure 1 describes mean rank and shows that the group without VD had a higher score than group with VD. But for condition 1 of mCTSIB it is shown that the violin plot has no any differences for mean, median score and inter quartile range (IQR). There were 25% the data value in condition 1 show had the same score between group 1 and 2. The upper quartile explained condition 1 and 2 had the same score in both groups. However, the variability of the data for conditions 2 and 4 were higher in the group with VD. The variability of the data of mCTSIB total and condition 3 presented higher in the group without VD. Furthermore, Fig. 2 explains almost all the data had variability distribution, exception the TUG (both groups) and social participation had a higher probability density function in the group with VD. The variability of the data was higher in the group with VD for FGA, FE, LSA and WHOQoL, while, TUG and PSSS were higher in the group without VD. Interestingly, the data value about 25% also seemed for environmental domain (Fig. 3). No difference for inter quartile range (IQR) psychological and environmental domain for both groups. But, in the group without VD had higher variability of data for physical and social domain.

Discussion

This study showed the differences of balance performance, falls-efficacy, social participation and quality of life between individuals with T2DM with and without VD. Overall, the T2DM participants with VD had lower performance of balance and falls-efficacy, as well as reported poorer social participations and quality of life.

In this study, mostly the participation had duration of DM of 5–10 years. Komalasari et al. (2022) also reported the same result but different year and area (Komalasari & Arif, 2023). Both static and dynamic balance performances were evaluated by mCTSIB, TUG and FGA. All balance test results indicated lower ability in the group with VD. The mCTSIB has been used to detect balance impairment by specifically indicating sensory contributing for balance control (Wrisley & Whitney, 2004). There was no difference between groups for condition 1 but significant differences for total score as well as conditions 2, 3 and 4 in this study. This results also confirmed that the limited function of the vestibular system in patients with VD affected the balance performance. Condition 1 is a standard test where the person uses all three sensory systems available to maintain balance, and therefore the smallest amount of postural sway is expected (Goble et al., 2019). In condition 2, in which the participants stand on a firm surface with eyes closed, i.e., eliminating visual feedback, the proprioceptive and vestibular systems were delegated to detect the body position. This condition is postulated to measure the contribution of proprioception in balance mostly (Nashner, Black & Wall 3rd, 1982). In this study, the patients with VD had lower performance under condition 2 compared with the ones without VD. It should be noted that more than half of participants in both groups had DPN which might also be associated with the proprioceptive impairment. The violin plot (picture 1) which describes condition 2 also has the same median range and upper quartile in both groups. This result confirmed the VD patient could still stand on foam with eyes opened. The role of the visual system is very useful for stabilizing body position despite having limitations in the vestibular system. Gaze stabilization is the ability of individuals to focus their eyes when their head is moving (Crane & Demer, 1997). For condition 3, the participant was standing on foam with eyes open, so the proprioceptive was removed and the contributions of the visual and vestibular systems was made manifest. The participants with VD implicate the visual system by giving its preference over vestibular feedback for balance. Condition 4 of mCTSIB was standing on foam with eyes closed. In this case, the visual and proprioceptive functions are disturbed and shifting reliance on the vestibular function to maintain balance. People with VD find it difficult to maintain balance in this condition since it relies primarily on the vestibular input. Previous studies demonstrated that standing on foam with eyes closed was more challenging than standing on the floor, that subjects display greater postural sway (Goble et al., 2019). Also, another study reported that VD independently increased the risk of falling two-fold in DM patients assessed by the modified Romberg test. Most of participants failed in the condition 4 to determine vestibular function exclusively. The test instructs the subjects have to maintain balance on a foam-padded surface (to eliminate proprioceptive input) with their eyes closed (to block visual input) (Agrawal et al., 2010). Although DPN is the common impairment occurred in T2DM, VD impairment can occur in T2DM patients before they suffer with the DPN (Deshpande, Hewston & Aldred, 2017). Failure in conditions 3 and 4 were also suggested to be associated with decreased lower limb muscle strength as well as the poor balance confidence (Vongsirinavarat et al., 2020).

The results of dynamic balance tests indicated that T2DM with VD had lower dynamic balance performances measured by TUG and FGA, compared with the group without VD. The patients with high risk of falling recorded highly classified by TUG and FGA categories. The TUG evaluates balance during the walking and turning 180 degrees as well as transfers to and from a seated position (Podsiadlo & Richardson, 1991) which was more problematic and increased the risk for falls while turning for patients with VD. Also, the task of walking with head movements in FGA puts even more of a challenge on the vestibular system. A previous study stated that rotating the head to the right, left, up and down during ambulation was the most the difficult tasks of the FGA for subjects with VD (Shumway-Cook & Woollacott, 2010). The increased input from the cervical afferents that occurs while rotating the head during walking might conflict with the abnormal information being received in the vestibular nucleus, resulting from VD. Therefore, disruption of the sense of positions in space would occur (Cohen, 1961). The results might also imply that the FGA is a more sensitive tool compared with TUG to detect balance problems in persons with VD. Notably, the participants who considered high risk of falling were higher by FGA test than TUG test in two groups.

Furthermore, the mean of muscle strength in lower limb was lower in both groups especially the group with VD. The association between DM and muscle strength was explicit (Hong et al., 2017; Vongsirinavarat et al., 2020). The greater number of peripheral sensory impairments contributed to reducing muscle strength in ankle and knee movements, as well as significantly reduced mobility and function (Kraiwong et al., 2019). More than 80% of participants in this study also had cognitive impairment. In patients with DM, the neurophysiological changes occur due to hyperglycemia and the cognitive decline is evident, notably over 4–6 years after DM diagnosis (Jia et al., 2020). A previous study also reported that declined cognitive function could change the gait, imbalance and made the patients became the fallers (Taylor et al., 2013).

Regarding the FE, the T2DM patients with VD presented lower score of ABC-16 than without VD. The decreased FE was also proposed to be potentially more debilitating than a fall (Hewston & Deshpande, 2018). Previous studies found that neuropathic pain was a strong factor increased fear of falling in T2DM patients and obviously hamper the activities (Brod et al., 2015). In patients VD, mostly FE comes because of dizziness and feeling unstable when standing or doing some activities. Previous studies justified the effectiveness of gaze and balance exercises to improve balance and confidence respectively with moderate effect size (Aldawsary & Almarwani, 2023; Bhardwaj & Vats, 2014).

The participants with VD in this study were presented with greater limitations of social participation monitored by PSSS-Ina and LSA-Ina. The proportion of participants who were considered having severe restricted participation was also significantly greater. The symptoms associated VD specifically dizziness appeared to increase risk of imbalance and falls (Agrawal et al., 2010) and effect on functioning, especially on daily activities and social participation (Komalasari et al., 2022). Dizziness is also a condition inducing emotional stress increases isolation, reduces self-autonomy, and self-control as well worsening FE that might highlighted an increased in restriction and disability (Weidt et al., 2014). The patients tended to avoid activities, environments and situations that provoke the symptom, and required assistance to stand and ambulate, therefore making them more dependent (Lasisi & Gureje, 2010). Vestibular rehabilitation shows positive impact to reduce dizziness feeling and improve QoL significantly (Giray et al., 2009; Ribeiro et al., 2017)

Obviously, T2DM patients with VD showed significantly lower QoL presented by total score and the scores of all domains of WHOQoL. A previous study explained that DM patients had significantly reduced QoL due to many factors resulting from micro and macrovascular complications. The decreased balance control due to the deterioration of sensory, cognitive and musculoskeletal systems consequently impaired QoL (Dunsky, 2019). QoL was also consistently associated with a higher prevalence of disability in all states, as well as with a progression of disability states (Bourdel-Marchasson, Faqot-Campagna & J, 2007).

This study had some limitations. The VD condition was identified using clinical tests, i.e., the HIT, the DHT and the SRT. To confirm VD, at least one positive VD tests was used. The goggle glasses were not used to confirm the eyes saccades or nystagmus for all tests. Further studies might differentiate the types of VD and find the association with the balance performance, falls-efficacy, social participation and QoL. Also, the exploration in people without T2DM but having VD would add some confirmation of our findings. In addition, the contribution of psychological factors should add a more holistic approach to the issue of participation and QoL. A cross-sectional design like this study would show the occurrences of each factors that might be associated with the limitations of social engagement as well as the reduced QoL in participants with and without VD. Further studies exploring the contributions as well as the management which could prevent or improve the deterioration are warranted.

Conclusion

The ability to maintain balance declined, balance confidence and physical performances were found to reduced accompanied by the declined social participations and QoL in T2DM with VD compared to the group without VD. The VD complications need to be addressed in clinical settings. The comprehensive screening and management of vestibular dysfunction should be applied. The specific rehabilitation program of vestibular rehabilitation, balance and physical training should be encouraged to improve mobility and balance confidence as well as social participation.