Abstract
Background:
Diabetes is the most common cause of peripheral neuropathies. No definitive treatment for diabetic neuropathies has been reported, and very few studies have been published on the role of exercise in reducing either the symptoms or incidence of diabetic neuropathies.
Methods:
This study assessed the effects of an exercise program on balance and trunk proprioception in older adults with diabetic neuropathies. Thirty-eight patients with diabetes having peripheral neuropathies were enrolled, randomized, and subdivided in two groups: an experimental group of 19 participants with diabetes (72.9 ± 5.6 years old) and a control group of 19 participants with diabetes (73.2 ± 5.4 years old). Both groups received health education on diabetes for 50 min/week for 8 weeks. The experimental group practiced an additional balance exercise program for 60 min, two times a week. The exercise training was performed two times per week for 8 weeks. Results were evaluated by both static and dynamic balance and trunk proprioception.
Results:
Postural sway significantly decreased (P < 0.05), the one-leg stance test significantly increased (P < 0.05), and dynamic balance from the Berg Balance Scale, Functional Reach Test, Timed Up and Go test, and 10-m walking time improved significantly after balance exercise (P < 0.05). Trunk repositioning errors also decreased with training (P < 0.05).
Conclusion:
The balance exercise program improved balance and trunk proprioception. These results suggested that a balance exercise is suitable for individuals with diabetic neuropathy.
Introduction
As proprioception decreases, the ability to coordinate basic protective reflexes and joint movement as well as complex balance and postural control also decreases. 9 –12 Particularly in the elderly, muscle weakness, delayed reflex responses to sudden changes in posture, and asymmetric weight bearing due to impaired proprioception creates balance impairments. 13 Falls occurring due to impaired balance and unstable walking are the primary cause of early mortality in the elderly. 14 Furthermore, impaired balance in the elderly with diabetic neuropathy is a chief cause of increasing falls and decreasing quality of life. 15,16 Therefore, balance improvement in the elderly with diabetic neuropathies is very important for preventing falls and improving the quality of life. 17 Some studies have reported aerobic activity, core strength training, and flexibility exercises for improving balance in older people, 18 –24 and it is generally believed that exercise is effective in improving balance in the prevention of falls in the elderly. 25 However, although there are many studies that have examined the effects of an exercise program in improving glycemic control, insulin sensitivity, and other risk factors, there are very few studies that have been conducted on improving balance and gait function in patients with diabetic neuropathies. 26 Therefore, the purpose of this study was to assess the effects of a balance training exercise program on balance and trunk proprioception in the elderly with diabetic neuropathies.
Subjects and Methods
Subjects
Thirty-eight patients with diabetes diagnosed with diabetic peripheral neuropathies by a physician were recruited and randomly assigned to two groups: an experimental exercise group with 19 participants with diabetes (72.9 ± 5.6 years old) and a control group with 19 participants with diabetes (73.2 ± 5.4 years old). Exclusion criteria for all subjects were any musculoskeletal impairment, such as the inability to walk independently, manual muscle testing grade under 3 in the lower extremity, fracture or malformation, and severe osteoarthritis, neurological impairments in the central nervous system or vestibular system, postural hypotension, intellectual disabilities, and psychiatric disorders.
As shown in Table 1, there was no significant difference in age, sex, height, weight, blood glucose level, number of falls, number of exercises performed weekly, and duration of diabetes among both the groups. All experimental protocols and procedures were explained to each subject and approved by the Institutional Review Board of Sahmyook University. All subjects signed a consent form.
Statistical analysis
Statistical analysis was accomplished using SPSS version 17.0 software (SPSS, Inc., Chicago, IL). The data were analyzed by the Shapiro–Wilk test for normality. Descriptive statistics was used for demographics. Independent t test and the χ 2 test were used for maintaining homogeneity between the two groups. Paired t test was used to compare between pre- and post-test exercise measurements in both groups. The level of significance was P ≤ 0.05.
Interventions
Balance exercise
This exercise program (Table 2) was designed based on previous studies of exercise that has been shown to improve balance. 26,27 The exercise was conducted twice a week for 8 weeks. Each exercise comprised 10 min of warm-up activities, 40 min of balance training, and 10 min of cool-down activities. The exercises were performed in a group such that when one person was exercising, the other was supervising.
Warm-up exercises included gentle stretching, forward, backward, and sideways step-ups on foam, and massage with the sensory ball, all performed to light soothing music. 28 This warm-up was performed to increase flexibility of the muscles.
Balance exercises consisted of three parts. The first and second part comprised two sets of 4 min each, with eyes opened and eyes closed, respectively. In particular, while performing the second set, subjects were paired for their safety, and they performed it in turns. The third part included three activities to challenge and increase their balance. In the first activity, the subjects were asked to stand in a circle on foam and pass doughnuts from themselves to the next subject in the circle. The donuts were passed with the help of a straw in their mouths. The second activity was performed in pairs and comprised catching and throwing a ball while standing on the foam. The third activity was performed in a similar way but on a trampoline instead of on foam to challenge balance strategies. The size of the ball, the number of repetitions, and the distance between subjects were increased progressively as the patients' balance responses improved.
After every set of exercise, subjects were given a 2-min rest (especially during the first and second part), during which they performed upper limb exercises with a Thera-Band® sitting on a Thera-Band exercise ball (Hygenic Corp., Akron, OH). 29
Following balance training, cool-down exercises were performed to prevent muscle fatigue, sudden hypoglycemia, and relaxation of tensed muscles and to help bring the patients' heart rate and respiratory rate back to normal. These exercises included deep breathing, abdominal breathing, and static back extensor exercises and were performed in a reclined position. 30
An oval-shaped foam (Thera-Band Stability trainer, soft blue), measuring 40.64 × 22.86 × 5.08, and a small soft ball (Edufom, Incheon, Korea), 120 mm in diameter made up of polyurethane foam, were used. The red Thera-Band gym ball, 55 cm in diameter, made up of polyvinyl chloride, provided adequate bouncing and durability and was thus used effectively and safely. The yellow Thera-Band was 40 cm in length and provided a resistance of 1 kg.
Health education for diabetes
Health education was conducted once a week for 8 weeks with each session lasting 50 min. This education was delivered by a professional nurse specialized in diabetic education and another individual specialized in physical education.
The goal of this comprehensive and systematically given diabetes education was to create awareness among the older subjects with diabetes to manage the disease and to find ways to prevent its complications. The content of this education was systematically divided into 8 weeks. The first and second week focused on definition, disease process, and the importance of diet and exercise. The third and fourth week included the diet plan and insight on the complications of diabetes. The fifth and sixth week included the importance of exercise therapy in management in diabetes. The last 2 weeks provided a summary of the previously given education and stepwise integrative approach to the management of diabetes.
Outcome measures
Multifunction force measuring plate
The Zebris multifunction force measuring plate (Zebris Medical GmbH, Isny, Germany) operated with 1,504 capacitive force sensors arranged in a 32- × 47-cm matrix. It allowed for analysis of the static and dynamic force and pressure distribution under the feet/shoes when standing and walking. For analysis, evaluation of the data measured took place directly after the measurement. The measures were available in the shortest possible time frame by way of a “Report.” The PDM system consisted of a multifunction force measuring plate, with a special connecting board integrated in the Zebris motion analysis system. The measuring system was able to show two- and three-dimensional displays of the static load distribution in real time. The left foot and the right foot, as well as the front and back foot percentage load distributions, were presented as a bar chart, which thereby provided a direct comparison. The subjects stood comfortably on the platform without shoes in a quiet stance position. The feet were kept at a parallel distance of approximately 10 cm between them. First, the subjects were tested with their eyes open and then with eyes closed. The duration of the measurement was 30 s. During the quiet stance the total excursion of the center of pressure was recorded. Data were gathered three times with a rest period of 3 min between each measurement to prevent muscle fatigue.
One-leg standing test
The one-leg standing (OLS) test assesses static balance ability in standing. 31,32 OLS tests were measured on dominant and nondominant legs in three positions: eyes open (60 s), eyes closed (30 s), and eyes open with head rotation (30 s). Subjects were allowed one practice trial for each of the balance tests. The test was accepted as failure when the stance foot shifted in any way or the non-stance foot touched the ground. Each subject performed three trials, and the best result of the three trials was recorded.
Berg balance scale
The Berg Balance Scale (BBS) was developed to measure balance among older people with impairment in balance by assessing the performance of functional tasks; it is a valid instrument used for evaluation of the effectiveness of interventions and for quantitative descriptions of function in clinical practice and research. 33 The balance assessment consists of 14 tasks performed in a standard order. Each task is scored on a 5-point scale (0–4) according to the quality of the performance or the time taken to complete the task, as ranked by the test developers. The maximum score for this assessment is 56. A score below 45 indicate impairment, with an increased risk for falls. The tests have high intra-rater reliability (0.99) and inter-rater reliability (0.98). Therefore, for assessing balance, this test has high reliability and internal validity. 33,34
Functional Reach Test
The Functional Reach Test (FRT) assesses dynamic balance by measuring the maximum distance a subject can reach forward beyond one's own arm length while maintaining a fixed base of support in the standing position. 35 A yardstick is mounted on the wall at shoulder height. Subjects are asked to reach as far forward as possible in a plane parallel to the measuring device without taking a step forward. The better of the two trials is recorded, in centimeters. The FRT is a precise (coefficient of variation = 2.5%) and stable measure (intra-class correlation = 0.92) with established sensitivity to change (responsiveness index = 0.97). 35
Timed Up and Go test
The Timed Up and Go (TUG) test is a test of balance that is commonly used to examine functional mobility in community-dwelling, frail older adults. This test measures, in seconds, the time taken by an individual to stand up from a standard armchair (approximate seat height of 46 cm), walk a distance of 3 m, turn, walk back to the chair, and sit down. The subject wears his or her regular footwear and uses his or her customary walking aid (cane, walker, etc.). No physical assistance is given. Time taken to complete the test is strongly correlated to level of functional mobility. Older adults who are able to complete the task in less than 20 s have been shown to be independent in transfer tasks involved in activities of daily living and walk at gait speeds that should be sufficient for community mobility (0.5 m/s). In contrast, older adults requiring 30 s or longer to complete the task tend to be more dependent in activities of daily living and require assistive devices for ambulation. Three trials were performed and averaged. This test as a measure of physical mobility has good intra-rater and inter-rater reliability (r = 0.99 and 0.98, respectively). 36,37
10-m walking test
Walking speed was measured by timing subjects over a distance of 10 m with a stopwatch. To avoid the effects of acceleration and deceleration, measurements were taken over the middle 10 m of a 14-m walkway. 38 The three trials were performed and averaged for use in data analysis. Intra-rater and inter-rater reliabilities have been reported as high (r = 0.89–1.00). 39
Trunk repositioning errors
Trunk repositioning errors (TREs) is one of the most common tests to assess trunk proprioception. Testing took place with the patient standing under three visual-surface conditions: eyes open on stable surface, eyes closed on stable surface, and eyes open on foam. 40 To assess TREs, a digital inclinometer (Dualer IQ™, J-TECH Medical, Salt Lake City, UT) with accuracy of 1° and repeatability of 1° was used. It was held between the T12 and S1 vertebrae. Subjects flexed the trunk approximately 30° in the sagittal plane, holding the position for a count of 5 s. After returning to the upright position, subjects attempted to duplicate the previously attained angle. Subjects indicated verbally when they felt they had reached the angle and held their position for a count of 5 s. The absolute difference in degrees between the first position and second position was defined as the TRE. Subjects generated five scores for each visual-surface condition. For each condition, the highest and lowest scores were discarded, and the mean of the remaining three scores represented the TRE score.
Procedures
Subjects having diabetic neuropathy were recruited by physicians during a health education campaign. Subjects were interviewed for inclusion and exclusion criteria, and informed consent was taken. Subjects were then randomly divided into an exercise and control group. The balance exercise program was conducted for 8 weeks. Subjects were assessed 1 week after and before the balance exercise program. Before the exercise program, demographics and static, dynamic, and trunk proprioception were assessed by four different trained examiners. The examiners are all physical therapists who have practiced for over 10 years. In both groups, the subjects received health education for diabetes for 50 min once every week. Subjects in the exercise program received balance exercises for 60 min twice a week. The control group did not receive any balance exercises. Subjects were supervised by one researcher and three helpers. Three helpers supervised the subjects who could not perform their exercises correctly. Health education for diabetes was conducted by a professional health nurse. This education included topics of principles, diagnosis, diet plan, and management of its complications. All subjects were assessed again after completing 8 weeks of intervention.
During the study, some subjects dropped out as they did not wish to continue. Some subjects also withdrew because of medical conditions. Some subjects who participated in <80% of all exercises were dropped. In the exercise group, one subject dropped out because of complications of diabetes, while two subjects dropped out as they could not complete 80% of the exercises. Finally, 19 subjects participated in the study from the exercise group. In the control group three subjects were eliminated because they could not participate in 80% of the study. In total, 19 subjects participated in the study from the control group.
Results
Homogeneity test for balance and trunk proprioception
On pre-testing the subject, there was no difference between the control and exercise groups in balance and trunk proprioception. There was no significant difference in total body sway between both groups with their eyes open and eyes closed (P > 0.05, Table 3). Also, anterior–posterior and medial–lateral between the two groups with eyes open and eyes closed were not significantly different (P > 0.05, Table 3). On pretesting of the OLS test, there was no significant difference between both groups with their eyes open, eyes closed, and eyes open head rotation standing on either of the legs (P > 0.05, Table 3).
Data are mean ± SD values of the group.
BBS, Berg Balance Scale; EC stable surface, trunk repositioning errors on stable surface with eyes closed; ECAP, anterior–posterior body sway with eyes closed; ECLT, left leg standing with eyes closed; ECML, medial–lateral body sway with eyes closed; ECRT, right leg standing with eyes closed; ECTS, total body sway with eyes closed; EO foam, trunk repositioning errors on foam with eyes open; EO stable surface, trunk repositioning errors on stable surface with eyes open; EOAP, anterior–posterior body sway with eyes open; EOLT, left leg standing with eyes open; EOML, medial–lateral body sway with eyes open; EORT, right leg standing with eyes open; EOTS, total body sway with eyes open; FRT, Functional Reach Test; HRLT, left leg standing with eyes open and head rotation; HRRT, right leg standing with eyes open and head rotation; OLS, one-leg standing; TUG, Timed Up and Go test; 10-m walk, 10-m walking test.
On pretesting of dynamic balance using BBS, FRT, TUG, and 10-m walking test, there was no difference between the two groups (P > 0.05, Table 3).
On pretesting of TREs while performing trunk proprioception on a stable surface with eyes open and eyes closed and on the foam with eyes open, there was no difference between the two groups (P > 0.05, Table 3).
Changes in static balance
Static balance was assessed using body sway distance and one-leg stance (Table 4). On the body sway distance test, there was a significant difference in the exercise group between pre- and post-testing in all conditions (eyes open anterior–posterior, eyes closed anterior–posterior, eyes open medial–lateral, eyes closed medial–lateral, eyes open total body sway, and eyes closed total body sway) (P < 0.05). In the control group, however, there was no statistical difference in pre- and-post testing.
Data are mean ± SD values of the group.
*P < 0.05, **P < 0.01, ***P < 0.001.
AP, anterior–posterior; EC, eyes closed; EO, eyes open; HR, head rotation; ML, medial–lateral; TS, total body sway.
On the OLS test, there was a significant difference in the exercise group between pre- and post-testing on the left and right legs in three conditions (eyes open, eyes closed, and eyes open head rotation) (P < 0.05). In the control group there was no statistical difference in pre- and post-testing.
Changes in dynamic balance
Dynamic balance was assessed by BBS, FRT, TUG, and 10-m walk (Table 5). The BBS significantly increased in the exercise group (P < 0.001). In the control group, there was no significant difference in BBS on pre- and post-testing.
Data are mean ± SD values of the group.
**P < 0.01, ***P < 0.001.
BBS, Berg Balance Scale; FRT, Functional Reach Test; TUG, Timed Up and Go test; 10-m walk, 10-m walking time.
FRT distance significantly increased in the exercise group (P < 0.01). In the control group there was no significant difference in the FRT score on pre- and post-testing.
TUG time significantly decreased in the exercise group (P < 0.01). In the control group there was no significant difference in TUG on pre- and post-testing.
The 10-m walk time significantly decreased in the exercise group (P < 0.001). In the control group there was no significant difference in the 10-m time on pre- and post-testing.
Changes in trunk proprioception
Trunk proprioception was assessed under three conditions: eyes open stable surface, eyes closed stable surface, and eyes open on foam (unstable surface) (Table 6). In eyes open stable surface, TREs significantly decreased in the exercise group (P < 0.05). In the control groups, there was no significant difference in these errors on pre- and post-testing.
Data are mean ± SD values (in °) of the group.
*P < 0.05, **P < 0.01.
In eyes closed stable surface, TREs significantly decreased in the exercise group (P < 0.01). In the control group, there was no significant difference in these errors on pre- and post-testing.
In eyes open on foam (unstable surface), TREs significantly decreased in the exercise group (P < 0.01). In the control group there was no significant difference in these errors on pre- and post-testing.
Discussion
Peripheral neuropathy has been associated with balance impairments and repetitive falls. 41 Impaired balance, neurological control, and gait and muscle weakness in the aging process become more evident in older people with diabetic neuropathy. Postural instability in diabetic neuropathy patients is usually attributed to the lack of accurate proprioceptive feedback from the lower limbs. This combined effects leads to increased prevalence of falls in people with diabetes. 41 –43 To prevent falls and their complication, proper interventions are needed to increase balance and proprioceptive feedback.
In this research, we found that 8 weeks of balance exercises improved static and dynamic balance, which is critical to the prevention of falls in elderly people with diabetes. Many studies have shown that balance exercises improve ability of movement and balance in older people. 44 –47 According to Richardson et al., 26 3 weeks of balance exercises improved confidence of performing static and dynamic balance, including activities-specific balance, in the elderly. In a study by Lord et al., 25 exercise improved fall risk by 17.76%. Melzer et al. 48 stated that 3 months of balance exercises resulted in 64.2% improvement in balance and that it also significantly improved anterior–posterior body sway in older people. This study found similar results of improvements in anterior–posterior body sway but in people with diabetes (27.43%). Improvements in anterior–posterior body sway were greater than improvements in medial–lateral body sway as the balance exercises comprised activities in which the subject had to maintain balance by using ankle strategy. According to Winter et al. 49 ankle strategy improves the ability to control anterior–posterior body sway, thus supporting the results of our study. Medial–lateral body sway is associated more with repetitive falls than anterior–posterior body sway. 50,51 Thus, as we can see, significant improvements in medial–lateral body sway in the study may have contributed to reducing the possibility of repetitive falls.
Postural sway during static standing increases in proportion with age. It is greater in older people who have experienced falls earlier. 52 In the presence of impaired balance, increasing age decreases reaction time, delays the production of muscle power, and decreases the ability of neuromuscular control in the ankle. 53,54 Deficient control in static standing is closely related to ankle instability. Therefore, it is essential to include exercises that mainly incorporate the ankle strategy in order to improve balance. According to Richardson et al., 26 in older people with peripheral neuropathy, the ability to maintain static balance with the eyes open increased from 5.4 s to 11.6 s. Englund et al. 44 found the same results. This shows that balance exercises are effective in improving the ability to maintain static balance.
In this study the BBS, FRT, TUG test, and 10-m walking test were administered to assess dynamic balance. All four tests showed significant improvements in dynamic balance. In a 1-year study of older women, improvements were seen in BBS scores from 55.1 to 55.3 after exercise. 44 This study also showed improvements from 52.9 to 55.1 after exercise. Similar results have been reported in various other studies. 46,47 As our study consisted of young elderly, the age cannot be matched with studies that comprised old elderly and old-old elderly. Because of this and the ceiling effect that has been reported with BBS, we cannot compare the results with other studies.
Nitz and Choy 55 reported increases in FRT scores from 26.5 cm to 28.2 cm in older people with 10 weeks of balance exercises, whereas Richardson et al. 26 reported increases in FRT scores from 26.7 to 29.2 with 2 weeks of balance exercises. The present study showed greater improvements in FRT than the previous two studies.
TUG is a simple method that can assess functional activities without specialized equipments and training, and it can also be carried out in a small area. In normal adults without peripheral neuropathy, the time taken on TUG is under 10 s, whereas in adult men in their sixties, the score is between 8 to 13.1 s. Previous studies show that older subjects who take over 14 s are at an increased risk for falls. Also, those who take over 30 s are unable to move independently, thus limiting outdoor activities. 37 In this study, after the balance exercises, the time taken on TUG was reduced from 11.7 s to 10.2 s, that is, by 1.4 s. Thus, this shows decreased risk of falls in adult men who are in their sixties with balance exercises. Madureira et al. 46 and Liu-Ambrose et al. 45 showed similar results. Therefore, this study shows that balance exercises are an effective intervention for improving dynamic balance in elder persons with diabetic neuropathy. In this study, reduction of trunk proprioception was measured by TREs. According to de Noronha et al., 56 ankle sprain results in proprioceptive deficits, which in turn results in impaired balance. Goldberg et al. 57 stated that impaired trunk position sense decreases the ability to maintain balance, thus increasing the risk of falls. The study emphasized trunk position sense in rehabilitation training for increasing balance and muscle power.
This study also aimed at evaluating the effects of balance training on trunk proprioception. After administration of the TREs test, trunk proprioception improved in all the three conditions as follows: eyes open stable surface (39.9%), in eyes closed stable surface (62.6%), and in eyes open on the foam (41.7%). There are no studies that showed the effects of exercises on trunk proprioception so the results obtained from this study cannot be compared. We have shown that balance exercises improve trunk proprioception.
In previous studies of older people, subjects with diabetes and neuropathy were not excluded, and age matching was not done. It is difficult to compare the differences between this study and other studies. There are very few studies on the effect of exercise on diabetic neuropathy. It is therefore difficult to compare this with other studies. The sample size is small for this study so there may be limitations in generalizing the results to the entire older population with diabetic neuropathy. However, in this study, balance exercises have shown a positive effect by improving balance and trunk proprioception in older people with diabetic neuropathy. In the future, we need to develop different kinds of balance exercises and study these in depth to assess their effect on balance and proprioception and also on muscle strength and gait. So research studies should be done continuously to improve the quality of life and prevent falls by enhancement of function and gait in older people with diabetic neuropathy.
Conclusion
This study was designed to improve balance and prevent falls by addressing trunk balance and proprioception through balance exercises in older people with diabetic neuropathy. Balance exercises that could be performed easily in daily life were used in this study, and changes in the ability to maintain balance and trunk proprioception were measured. In the exercise group, significant changes were seen in static balance, dynamic balance, and trunk proprioception. However, in the control group there were no significant changes.
Through this study we have confirmed that balance exercises improve balance and trunk proprioception and also the ability to control body posture. In the future, different balance exercises should be developed to improve the quality of life and prevent falls in older people with diabetic neuropathy.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
