- Email: [email protected]
Comparison of Balance Ability Between Patients With Type 2 Diabetes and With and Without Peripheral Neuropathy
Original Research
Comparison of Balance Ability Between Patients With Type 2 Diabetes and With and Without Peripheral Neuropathy Kil-Byung Lim, MD, PhD, Dong Jun Kim, MD, PhD, Jeong-hyun Noh, MD, Jeehyun Yoo, MD, Jung-Wha Moon, PhD Objectives: (1) To examine the effects of peripheral neuropathy on balance stability in patients with type 2 diabetes, and (2) to assess static and dynamic balance and functional limitations. Design: A cross-sectional study. Setting: Outpatient clinic. Patients: Subjects with type 2 diabetes and healthy subjects (n ¼ 60) were divided into 3 groups: subjects with diabetes and with established peripheral neuropathy (diabetic peripheral neuropathy [DPN] group) (n ¼ 17), subjects with diabetes and without peripheral neuropathy (diabetic control group) (n ¼ 25), and subjects without diabetes (nondiabetic control [NDC] group) (n ¼ 18). Methods: Sensory impairment assessment, motor impairment assessment, and functional limitation assessment were assessed by using the Balance Master system. Results: In motor impairment assessment, left-to-right directional control in the rhythmic weight shift was significantly poorer in the diabetic control group than in the NDC group during slow movement (P ¼ .027). During fast movement, it was poorer in the DPN group than in the NDC group (P ¼ .022). In the unilateral stance test of functional limitation assessment with both eyes open, the mean center of gravity sway velocity was significantly higher in the DPN group than in the NDC group (P ¼ .011 for the left leg standing, P ¼ .008 for the right leg standing) and higher in the DPN group than in the diabetic control group (P ¼ .027 for the right leg standing). In the tandem walk test, walking speed was significantly lower in the DPN group than in the NDC group (P ¼ .033), and end sway was significantly greater in the DPN group than in the NDC group (P ¼ .020). Conclusions: Analysis of the results of this study suggest that functional limitations may occur more in the patients with diabetes and with peripheral neuropathy, and dynamic balance stability may decrease more with the patients with diabetes than with the subjects without diabetes. Further studies on balance rehabilitation that concern dynamic balance stabilities and exercise abilities are needed in patients with diabetes. PM R 2014;6:209-214
The incidence of diabetes has been increasing worldwide, especially in Asian countries where industrial advances have progressed rapidly. According to the World Health Organization report, 110.4 million persons had diabetes in the 1990s, 210 million persons had diabetes in the 2000s, and this number is predicted to increase to 299 million persons by 2025 [1]. Diabetes can cause retinopathy, renal failure, cardiovascular disease, and peripheral neuropathy. Aggressive control of blood glucose levels and concurrent diseases is mandatory to minimize such complications. Exercise has proved to be effective in the control of blood glucose levels and the prevention of complications, and is thus recommended as an important treatment method along with dietary therapy and pharmacotherapy [2]. Diabetic peripheral neuropathy (DPN) is the most common complication
1934-1482/13/$36.00 Printed in U.S.A.
D.J.K. Department of Endocrinology, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose J.-h.N. Department of Endocrinology, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose J.Y. Department of Rehabilitation Medicine, Inje University College of Medicine, Ilsanpaik Hospital, 170 Joohwaro, Ilsanseo-gu, Goyangsi, Gyeonggi-do, South Korea. Address correspondence to: J.Y.; e-mail: [email protected] Disclosure: nothing to disclose
INTRODUCTION
PM&R
K.-B.L. Department of Rehabilitation Medicine, Ilsanpaik Hospital, Inje University, Gyeonggido, South Korea Disclosure: nothing to disclose
J.-W.M. MS Sports Medicine Center, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose This work was supported by a 2009 Inje University research grant. Peer reviewers and all others who control content have no relevant financial relationships to disclose. Submitted for publication January 14, 2013; accepted November 14, 2013.
ª 2014 by the American Academy of Physical Medicine and Rehabilitation Vol. 6, 209-214, March 2014 http://dx.doi.org/10.1016/j.pmrj.2013.11.007
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among microvascular diseases and can reduce quality of life, and may be the main cause of nontraumatic amputation [3]. Patients with DPN frequently present with numbness and pain in the extremities due to decreases in peripheral nerve function and with balance instability due to decreases in proprioceptive functions. Because walking velocity and step width decrease more in patients with diabetes and with DPN than in those without DPN, patients with diabetes and with DPN are at high risk of falling [4,5]. In addition, decreases in movement perception of the hip and ankle joints can induce static and dynamic balance instabilities and thus increase the risk of falling [6-8]. Falling can increase morbidity and mortality by causing femur and ankle fractures, cerebral concussions, and cerebral hemorrhages. In addition, fear about falling decreases willingness to walk; inhibits exercise and/or physical activities, which are effective methods for blood glucose control; lowers quality of life through muscle weakness, postural instability, and gait abnormalities; and increases the incidence of secondary injuries associated with falling. An early detection of DPN, along with adequate management and training for balance impairment, can help decrease instances of falling. Many studies have been published about balance ability in patients with diabetes, and they have mostly focused on the relationship between DPN and balance ability [5,8-11]. Few studies have compared balance ability in patients with diabetes and with and without peripheral neuropathy [6,12,13]. There have been no comparative studies that used the Balance Master system (NeuroCom Inc, Clackamas, OR) to evaluate sensory impairment, motor impairment, and functional limitation to compare patients with DPN with patients with diabetes and without peripheral neuropathy. Therefore, this study was conducted to quantitatively measure balance stability and to compare the results among patients with diabetes and with DPN, patients without DPN, and healthy subjects.
BALANCE IN PATIENTS WITH AND WITHOUT DPN
DPN Evaluation After informed consent, all the subjects underwent nerve conduction studies of the bilateral lower extremities by using Neuroscreen Plus (Jaeger-Toennies, Freiburg, Germany). The sural and superficial peroneal nerve for sensory nerve and the posterior tibial and peroneal nerve for motor nerve were tested. Mean values of onset latencies and amplitudes of each nerve were calculated, and mean nerve conduction velocities also were calculated in case of motor nerves. Normal reference values of each nerve were based on the manual by Lee and DeLisa [14]. All the subjects also were evaluated by the Michigan Neuropathy Screening Instrument (MNSI), which consists of 2 assessments: part 1 is a 15-item self-administered questionnaire scored by summing abnormal responses, and part 2 is a physical examination of the lower extremities that includes inspection and assessment of fine touch, vibration sensation, and ankle reflexes. MNSI is scored by assigning points for abnormal findings. DPN was defined as present based on the following: (1) if subjects showed any abnormality in sensory and/or nerve conduction studies, and (2) if subjects had 7 or more positive responses on the MNSI questionnaire or a score of >2.0 on the MNSI examination [15]. The subjects were divided into 2 groups based on the results of their nerve conduction studies and MNSI. The subjects who were diagnosed as DPN were placed in the DPN group (n ¼ 17), and the other subjects were placed in the diabetic control (DC) group (n ¼ 25). There were no significant differences in gender, age, height, or body weight between the 2 groups. However, disease duration from diagnosis to the commencement of this study and the types of medication administered at the time of the study were significantly different between the DPN and DC groups (P ¼ .001, P ¼ .021, respectively) (Table 1).
Balance Stability Evaluation METHODS Study Subjects This study included 42 subjects with type 2 diabetes mellitus who were older than 40 years of age and were recruited from the Departments of Rehabilitation Medicine and Endocrinology at our hospital. All provided signed informed consent. Exclusion criteria were the following: a history of cardiovascular disease, orthopedic disease, renal dysfunction (serum creatinine level, 2.0 mg/dL), hepatic dysfunction (aspartate transaminase or alanine transaminase level, 40 IU/L), or other life-threatening diseases; having been medicated with gabapentin, pregabalin, or thioctic acid for pain control; and having been medicated with antipsychotic agents. Eighteen adults without diabetes, ages 40 years old or older, who met the same exclusion criteria as the subjects with diabetes were brought in as the control group (nondiabetic control [NDC] group).
Balance stability was separately assessed by using the Balance Master system after complete description of test procedures to each participant. All the participants then underwent sensory impairment assessment (SIA), tests of static balance stability and motor impairment assessment (MIA), tests of dynamic balance stability, and functional limitation assessment (FLA), as they stood in front of the monitor of the Balance Master system. Because different features of their own shoes, for example, thickness of their soles, would have influenced test results, the participants were asked to wear special shoes fitted for their feet, which were provided by the balance test laboratory (Figure 1).
SIA SIA was performed by using modified clinical test sensory interaction on balance (mCTSIB). All the subjects were asked to stand on the foam-covered force plate of the test machine,
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Table 1. General characteristics of the subjects
Total subjects, n Gender, n Men Women Mean SD age, y Mean SD height, cm Mean SD weight, kg Mean SD duration after diagnosis of DM, y Management for DM, n subjects Single oral medication 2 Kinds of oral medication 3 Kinds of oral medication Oral medication with insulin Insulin only
DPN
DC
NDC
17
25
18
8 9 60.0 11.2 161.8 8.7 69.2 9.6 8.8 5.0
13 12 55.5 8.2 160.5 7.1 65.0 9.9 4.0 3.0
7 11 52.0 6.8 159.7 6.5 60.4 8.8
1 10 0 5 1
10 10 3 2 0
DPN ¼ diabetic peripheral neuropathy; DC ¼ diabetic control; NDC ¼ nondiabetic control; SD ¼ standard deviation; DM ¼ diabetes mellitus.
and to maintain their standing posture with their eyes open for 10 seconds and again with their eyes closed for 10 seconds. Center of gravity (COG) sway velocity ( /s) was measured.
MIA MIA was performed by using the rhythmic weight shift test, a test of lefteright and fronteback COG shifts. We measured on-axis velocity and directional control according to the moving velocity (slow or fast). Slow moving was defined as 3-second transition, and fast moving was defined as 1-second transition. On-axis velocity reflects a dynamic body weight shift in an intended movement direction; the data were expressed as /s. Directional control reflects the degree of sway from a linear movement; the data were expressed as percentages.
FLA FLA was performed by using sit-to-stand, unilateral stance, tandem walk, and stepequick turn tests. In the sit-to-stand test, all the subjects were asked to place their feet on a mark on the force plate and to sit with their hip and knee joints flexed at 90 ; then they were instructed to stand while leaning their trunk forward. We measured weight transfer, rising index (the amount of force exerted by the legs during the rising phase), COG sway velocity (the control of the COG over the base of support during the rising phase and for 5 seconds thereafter), and lefteright weight symmetry (differences in weight between both legs while standing). In the unilateral stance test, all the subjects were asked to stand on 1 leg for 10 seconds on the power plate with their eyes open or closed, after which mean COG sway velocity was
Figure 1. Balance ability evaluation performed by using the Balance Master system. (A) Patients stood on the force plate for this study. (B) Sensory impairment assessment was performed by using modified clinical test sensory interaction on balance; patients stood on the foam-covered force plate. (C) Motor impairment assessment was performed by using the rhythmic weight shift. Patients tried to move the pointer to the target spot when they moved their body from left to right or from forward to backward. (D) Functional limitation assessment consisted of sit-to-stand, unilateral stance, tandem walk and stepequick turn tests.
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BALANCE IN PATIENTS WITH AND WITHOUT DPN
Table 2. Comparison of sensory impairment assessment within groups by using the mean center of gravity sway velocity ( /s)
Eye open, median (min-max) Eye closed, median (min-max)
DPN
DC
NDC
P Value
0.50 (0.3 to w1.2) 1.00 (0.6 to w1.5)
0.40 (0.2 to w0.8) 0.90 (0.6 to w1.8)
0.40 (0.2 to w0.6) 1.00 (0.4 to w1.5)
.460 .652
DPN ¼ diabetic peripheral neuropathy; DC ¼ diabetic control; NDC ¼ nondiabetic control; min ¼ minimum; max ¼ maximum.
measured. In the tandem walk test, all the subjects were asked to walk heel to toe along a central line. The measured parameters of the tandem walk test were as follows: step width (the lateral distance between the left and right feet on successive steps), walking speed, and end sway (the velocity of the anterioreposterior component of COG sway for 5 seconds beginning when the patient terminated walking). In the stepequick turn test, all the subjects were asked to take 2 steps forward, then turn 180 and return to the starting point. At that moment, we also measured their turn time (the amount of time required to execute the 180 in-place turn) and turn sway degree (the degree of body axis sway during their turn performance). For each test, 3 measurements were made, and the mean was calculated.
Statistical Analysis All statistical analyses were performed by using the SAS program (SAS Institute Inc, Cary, NC). Because the data in this study did not follow normal distribution, nonparametric tests were used. The Kruskal-Wallis test was used for comparing within 3 groups, and the Mann-Whitney U test was used for comparing between 2 groups. A P value of <.05 was considered statistically significant.
RESULTS SIA There were no significant differences in COG sway velocity with eyes open or closed among the 3 groups (Table 2).
MIA In the rhythmic weight shift test, on-axis velocity was not significantly different among the 3 groups. However, left-toright directional control in the rhythmic weight shift was significantly poorer in the DC group than in the NDC group during slow movement (P ¼ .027). During fast movement, it was poorer in the DPN group than in the NDC group (P ¼ .022) (Table 3).
FLA There were no significant differences in the results of the sit-tostand test among the 3 groups. In the unilateral stance test with both eyes open, the mean COG sway velocity was significantly higher in the DPN group than in the NDC group (P ¼ .011 for the left leg standing, P ¼ .008 for the right leg standing). When participants stood on their right leg with both eyes open, the
mean COG sway velocity was significantly higher in the DPN group than in the DC group (P ¼ .027). In the tandem walk test, walking speed was significantly lower in the DPN group than in the NDC group (P ¼ .033), and end sway was significantly greater in the DPN group than in the NDC group (P ¼ .020). There were no significant differences in stepequick turn among the 3 groups (Table 4).
DISCUSSION Balance control is affected by several factors, such as vision, proprioception, vestibular function, cerebellar function, and the muscle power of both lower extremities [16]. DPN decreases proprioception and induces numbness of the lower extremities, which leads to balance impairment [17,18]. In this study, we attempted to quantitatively evaluate balance abilities of patients with diabetes by using the Balance Master system. This instrument quantitatively assesses balance control and offers objective assessments of sensory impairment, motor impairment, and functional limitations [19]. SIA is the assessment of static balance ability when using mCTSIB. There was no difference among the 3 groups in tests in which the subjects had their eyes open or closed. However, in unilateral stance tests in the FLA, which also assesses static balance, the DPN group showed more balance instability than the NDC group when participants stood on their left leg. The DPN group also demonstrated more balance instability than both the DC and the NDC groups when participants stood on their right leg. In all cases, participants had their eyes open. It is commonly known that patients with DPN have static balance instability that is worse when visual feedback is eliminated. In this study, however, there was no difference among the 3 groups when participants performed unilateral standing with their eyes closed. Both mCTSIB and unilateral stance are static balance assessments, but unilateral stance is a more dynamic test than mCTSIB. The influence of DPN on static balance stability is minimal, and thus the mCTSIB test did not show any significant differences. However, the unilateral stance test, which is more difficult, can reveal instability. MIA is the assessment of dynamic balance ability, especially coordinated movements. In the MIA, the results of the left-to-right directional control test were significantly poorer in the DC group than in the NDC group during slow movement. During fast movement, the results were worse in the DPN group than in the NDC group. It is noteworthy that the subjects with diabetes, regardless of peripheral neuropathy, have dynamic balance instability compared with normal subjects. It is estimated that a marked decrease in directional control can increase the risk of falling and its
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Table 3. Comparison of motor impairment assessment by using the rhythmic weight shift test within groups DPN, median (min to wmax)
DC, median (min to wmax)
NDC, median (min to wmax)
3.2 (2.2 to w4.3) 78 (51 to w85)
3.1 (2.2 to w3.8) 79 (64 to w88)*
3.1 (2.5 to w4.4) 75.5 (54 to w82)*
9.6 (5.7 to w13.7) 89 (83 to w95)*
8.6 (3.0 to w13.3) 89 (77 to w95)
7.6 (3.9 to w14.8) 86.5 (78 to w92)*
2.1 (1.5 to w3.8) 76 (53 to w86)
2.1 (1.6 to w2.9) 80 (51 to w87)
2.1 (1.8 to w3.2) 80.55 (64 to w86)
5.7 (2.1 to w8.6) 83 (61 to w95)
5.1 (2.3 to w7.5) 84 (65 to w94)
5.1 (3.1 to w7.4) 85.5 (74 to w92)
Left-right Slow On-axis velocity, /s Directional control, % Fast On-axis velocity, /s Directional control, % Forward-backward Slow On-axis velocity, /s Directional control, % Fast On-axis velocity, /s Directional control, %
DPN ¼ diabetic peripheral neuropathy; min ¼ minimum; max ¼ maximum; DC ¼ diabetic control; NDC ¼ nondiabetic control. *Significant differences, P < .05.
associated injuries. In our study, we found that left-to-right sway was significantly poorer in the DPN and DC groups than in the NDC group. However, there was no significant difference in the forward-to-backward sway test. A previous study revealed postural instability in patients with DPN, especially in the mediolateral direction [10]. Furthermore, our study showed that mediolateral stability also is lower in subjects with diabetes and without neuropathy. Maki et al [20] showed that left-to-right falling increases the risk of hip joint fractures more than does forward-to-backward falling. According to the previous study and results of this study, the risk of falling may be greater in the patients with diabetes,
regardless of peripheral neuropathy, than in normal subjects. Therefore, although clinicians have focused on balance training in patients with diabetes and with peripheral neuropathy, clinicians should recognize the necessity of early balance training for the prevention of falling even in patients with diabetes and without peripheral neuropathy. In the tandem walk in the FLA, the walking speed was significantly slower and end sway was significantly greater in the DPN group than in the NDC group. In a previous study, tandem stand was worse in the diabetic groups than in the NDC group [6]. Decreased proprioception, weak muscle power, and decreased somatoreceptor function lead to
Table 4. Comparison of functional limitation assessment within groups DPN, median (min to wmax) Sit-to-stand Weight transfer, s Rising index, % COG sway velocity, /s Left-right weight symmetry, % Unilateral stance, mCOG sway velocity, /s With both eyes open Left leg standing Right leg standing With both eyes closed Left leg standing Right leg standing Tandem walk Step width, cm Walking speed, cm/s End sway, /s Stepequick turn test Left turn time, s Right turn time, s Left turn sway, degree Right turn sway, degree
0.6 19.0 2.1 8.0
(0.2 to w1.9) (11.0 to w41.0) (0.8 to w4.8) (1.0 to w22.0)
DC, median (min to wmax) 0.4 23.0 3.0 4.0
(0.3 (8.0 (0.8 (1.0
to to to to
w1.2) w48.0) w5.0) w37.0)
NDC, median (min to wmax) 0.5 24.0 2.5 6.0
(0.2 to w1.6) (15.0 to w31.0) (0.8 to w3.6) (3.0 to w24.0)
1.0 (0.4 to w4.7)* 0.9 (0.5 to w8.3)*y
0.7 (0.3 to w4.5) 0.7 (0.5 to w4.4)y
0.6 (0.3 to w1.8)* 0.7 (0.4 to w1.7)*
2.0 (0.9 to w8.4) 1.5 (1.0 to w6.7)
1.7 (1.2 to w5.1) 1.7 (1.2 to w8.7)
1.4 (0.8 to w3.2) 2.1 (0.8 to w5.2)
6.5 (4.4 to w10.2) 23.8 (16.4 to w38.4)* 4.4 (2.7 to w6.8)* 1.1 0.9 21.6 21.9
(0.5 to w2.0) (0.5 to w2.4) (15.0 to w33.7) (16.0 to w30.3)
6.3 (4.6 to w9.2) 26.4 (13.2 to w43.6) 3.9 (1.2 to w7.9) 0.7 0.8 20.0 20.0
(0.3 to w1.2) (0.3 to w1.4) (12.7 to w29.2) (9.0 to w33.1)
6.2 (4.9 to w9.5) 29.2 (20.8 to w34.3)* 3.4 (2.5 to w5.7)* 0.7 0.9 19.7 22.0
(0.3 to w1.8) (0.4 to w2.3) (9.9 to w37.5) (12.0 to w32.4)
DPN ¼ diabetic peripheral neuropathy; min ¼ minimum; max ¼ maximum; DC ¼ diabetic control; NDC ¼ nondiabetic control; COG ¼ center of gravity; mCOG ¼ mean center of gravity. *Significant differences, P < .05, comparison between DPN and NDC group. y Significant differences, P < .05, comparison between DPN and DC group.
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postural abnormalities, which increase left-to-right weight sway, decrease walking speed, and elevate step-width while walking; and, when the base of support is fixed and small, dynamic balance is worse [10]. The results of this study indicate that the absence or presence of peripheral neuropathy may affect balance control in patients with diabetes and that balance abnormalities related to specific movements can be induced in patients with diabetes and with peripheral neuropathy. In addition, we were able to quantify static, dynamic, and functional balance abnormalities. Comparative analyses of the effects of diabetes on balance stability have implications in clinical practice. Balance exercise programs are necessary for patients with diabetes to improve dynamic balance stability and to minimize the functional limitation of specific movements.
CONCLUSIONS This comparative study of balance stability between patients with diabetes and normal subjects demonstrated that balance stability related to functional limitations in specific movements decreased more significantly in patients with diabetes and with peripheral neuropathy than in patients with diabetes and without peripheral neuropathy or in normal subjects. We also found that dynamic balance control was significantly worse in patients with diabetes and without peripheral neuropathy than in normal subjects. Further studies of dynamic balance stability and functional limitation of specific movements in patients with diabetes are needed to develop balance exercise programs.
REFERENCES 1. Amos AF, McCarty DJ, Zimmet P. The rising global burden of diabetes and its complications: Estimates and projections to the year 2010. Diabet Med 1997;14(Suppl 5):S1-S85. 2. European Diabetes Policy Group 1999. A desktop guide to type 2 diabetes mellitus. Diabet Med 1999;16:716-730. 3. Rathur HM, Boulton AJ. Recent advances in the diagnosis and management of diabetic neuropathy. J Bone Joint Surg Br 2005;87: 1605-1610. 4. Allet L, Armand S, de Bie RA, et al. Gait alterations of diabetic patients while walking on different surfaces. Gait Posture 2009;29: 488-493. 5. Menz HB, Lord SR, St George R, Fitzpatrick RC. Walking stability and sensorimotor function in older people with diabetic peripheral neuropathy. Arch Phys Med Rehabil 2004;85:245-252.
BALANCE IN PATIENTS WITH AND WITHOUT DPN
6. Resnick HE, Stansberry KB, Harris TB, et al. Diabetes, peripheral neuropathy, and old age disability. Muscle Nerve 2002;25:43-50. 7. Strotmeyer ES, de Rekeneire N, Schwartz AV, et al. Sensory and motor peripheral nerve function and lower-extremity quadriceps strength: The health, aging and body composition study. J Am Geriatr Soc 2009; 57:2004-2010. 8. Morrison S, Colberg SR, Mariano M, Parson HK, Vinik AI. Balance training reduces falls risk in older individuals with type 2 diabetes. Diabetes Care 2010;33:748-750. 9. Morrison S, Colberg SR, Parson HK, Vinik AI. Relation between risk of falling and postural sway complexity in diabetes. Gait Posture 2012;35: 662-668. 10. Ghanavati T, Shaterzadeh Yazdi MJ, Goharpey S, Arastoo AA. Functional balance in elderly with diabetic neuropathy. Diabetes Res Clin Pract 2012;96:24-28. 11. Maurer MS, Burcham J, Cheng H. Diabetes mellitus is associated with an increased risk of falls in elderly residents of a long-term care facility. J Gerontol A Biol Sci Med Sci 2005;60:1157-1162. 12. Emam AA, Gad AM, Ahmed MM, Assal HS, Mousa SG. Quantitative assessment of posture stability using computerised dynamic posturography in type 2 diabetic patients with neuropathy and its relation to glycaemic control. Singapore Med J 2009;50:614-618. 13. Turcot K, Allet L, Golay A, Hoffmeyer P, Armand S. Investigation of standing balance in diabetic patients with and without peripheral neuropathy using accelerometers. Clin Biomech (Bristol, Avon) 2009; 24:716-721. 14. Lee H, DeLisa J. Manual of Nerve Conduction Study and Surface Anatomy for Needle Electromyography. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005. 15. Moghtaderi A, Bakhshipour A, Rashidi H. Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg 2006;108:477-481. 16. Horak F. Clinical measurement of postural control in adults. Phys Ther 1987;67:1881-1885. 17. Lafond D, Corriveau H, Prince F. Postural control mechanisms during quiet standing in patients with diabetic sensory neuropathy. Diabetes Care 2004;27:173-178. 18. Akbari M, Jafari H, Moshashaee A, Forugh B. Do diabetic neuropathy patients benefit from balance training? J Rehabil Res Dev 2012;49:333-338. 19. Lim KB, Lee HJ, Joo SJ, Lim SS. Postural control measures of patients with back pain using Balance Master System. J Korean Acad Rehab Med 2007;31:30-36. 20. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol 1994;49:M72-M84.
This journal-based CME activity is designated for 1.0 AMA PRA Category 1 Credit and can be completed online at www.me.aapmr.org. This activity is FREE to AAPM&R members and available to non-members for a nominal fee. For assistance with claiming CME for this activity, please contact (847) 737-6000.
CME Question Diabetics, both with and without peripheral neuropathy, were more impaired than nondiabetics in: a. b. c. d.
forward to backward sway. tandem gait walking speed. left right directional control. unilateral stance testing.
Answer online at me.aapmr.org
Comparison of Balance Ability Between Patients With Type 2 Diabetes and With and Without Peripheral Neuropathy Kil-Byung Lim, MD, PhD, Dong Jun Kim, MD, PhD, Jeong-hyun Noh, MD, Jeehyun Yoo, MD, Jung-Wha Moon, PhD Objectives: (1) To examine the effects of peripheral neuropathy on balance stability in patients with type 2 diabetes, and (2) to assess static and dynamic balance and functional limitations. Design: A cross-sectional study. Setting: Outpatient clinic. Patients: Subjects with type 2 diabetes and healthy subjects (n ¼ 60) were divided into 3 groups: subjects with diabetes and with established peripheral neuropathy (diabetic peripheral neuropathy [DPN] group) (n ¼ 17), subjects with diabetes and without peripheral neuropathy (diabetic control group) (n ¼ 25), and subjects without diabetes (nondiabetic control [NDC] group) (n ¼ 18). Methods: Sensory impairment assessment, motor impairment assessment, and functional limitation assessment were assessed by using the Balance Master system. Results: In motor impairment assessment, left-to-right directional control in the rhythmic weight shift was significantly poorer in the diabetic control group than in the NDC group during slow movement (P ¼ .027). During fast movement, it was poorer in the DPN group than in the NDC group (P ¼ .022). In the unilateral stance test of functional limitation assessment with both eyes open, the mean center of gravity sway velocity was significantly higher in the DPN group than in the NDC group (P ¼ .011 for the left leg standing, P ¼ .008 for the right leg standing) and higher in the DPN group than in the diabetic control group (P ¼ .027 for the right leg standing). In the tandem walk test, walking speed was significantly lower in the DPN group than in the NDC group (P ¼ .033), and end sway was significantly greater in the DPN group than in the NDC group (P ¼ .020). Conclusions: Analysis of the results of this study suggest that functional limitations may occur more in the patients with diabetes and with peripheral neuropathy, and dynamic balance stability may decrease more with the patients with diabetes than with the subjects without diabetes. Further studies on balance rehabilitation that concern dynamic balance stabilities and exercise abilities are needed in patients with diabetes. PM R 2014;6:209-214
The incidence of diabetes has been increasing worldwide, especially in Asian countries where industrial advances have progressed rapidly. According to the World Health Organization report, 110.4 million persons had diabetes in the 1990s, 210 million persons had diabetes in the 2000s, and this number is predicted to increase to 299 million persons by 2025 [1]. Diabetes can cause retinopathy, renal failure, cardiovascular disease, and peripheral neuropathy. Aggressive control of blood glucose levels and concurrent diseases is mandatory to minimize such complications. Exercise has proved to be effective in the control of blood glucose levels and the prevention of complications, and is thus recommended as an important treatment method along with dietary therapy and pharmacotherapy [2]. Diabetic peripheral neuropathy (DPN) is the most common complication
1934-1482/13/$36.00 Printed in U.S.A.
D.J.K. Department of Endocrinology, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose J.-h.N. Department of Endocrinology, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose J.Y. Department of Rehabilitation Medicine, Inje University College of Medicine, Ilsanpaik Hospital, 170 Joohwaro, Ilsanseo-gu, Goyangsi, Gyeonggi-do, South Korea. Address correspondence to: J.Y.; e-mail: [email protected] Disclosure: nothing to disclose
INTRODUCTION
PM&R
K.-B.L. Department of Rehabilitation Medicine, Ilsanpaik Hospital, Inje University, Gyeonggido, South Korea Disclosure: nothing to disclose
J.-W.M. MS Sports Medicine Center, Ilsanpaik Hospital, Inje University, Gyeonggi-do, South Korea Disclosure: nothing to disclose This work was supported by a 2009 Inje University research grant. Peer reviewers and all others who control content have no relevant financial relationships to disclose. Submitted for publication January 14, 2013; accepted November 14, 2013.
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among microvascular diseases and can reduce quality of life, and may be the main cause of nontraumatic amputation [3]. Patients with DPN frequently present with numbness and pain in the extremities due to decreases in peripheral nerve function and with balance instability due to decreases in proprioceptive functions. Because walking velocity and step width decrease more in patients with diabetes and with DPN than in those without DPN, patients with diabetes and with DPN are at high risk of falling [4,5]. In addition, decreases in movement perception of the hip and ankle joints can induce static and dynamic balance instabilities and thus increase the risk of falling [6-8]. Falling can increase morbidity and mortality by causing femur and ankle fractures, cerebral concussions, and cerebral hemorrhages. In addition, fear about falling decreases willingness to walk; inhibits exercise and/or physical activities, which are effective methods for blood glucose control; lowers quality of life through muscle weakness, postural instability, and gait abnormalities; and increases the incidence of secondary injuries associated with falling. An early detection of DPN, along with adequate management and training for balance impairment, can help decrease instances of falling. Many studies have been published about balance ability in patients with diabetes, and they have mostly focused on the relationship between DPN and balance ability [5,8-11]. Few studies have compared balance ability in patients with diabetes and with and without peripheral neuropathy [6,12,13]. There have been no comparative studies that used the Balance Master system (NeuroCom Inc, Clackamas, OR) to evaluate sensory impairment, motor impairment, and functional limitation to compare patients with DPN with patients with diabetes and without peripheral neuropathy. Therefore, this study was conducted to quantitatively measure balance stability and to compare the results among patients with diabetes and with DPN, patients without DPN, and healthy subjects.
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DPN Evaluation After informed consent, all the subjects underwent nerve conduction studies of the bilateral lower extremities by using Neuroscreen Plus (Jaeger-Toennies, Freiburg, Germany). The sural and superficial peroneal nerve for sensory nerve and the posterior tibial and peroneal nerve for motor nerve were tested. Mean values of onset latencies and amplitudes of each nerve were calculated, and mean nerve conduction velocities also were calculated in case of motor nerves. Normal reference values of each nerve were based on the manual by Lee and DeLisa [14]. All the subjects also were evaluated by the Michigan Neuropathy Screening Instrument (MNSI), which consists of 2 assessments: part 1 is a 15-item self-administered questionnaire scored by summing abnormal responses, and part 2 is a physical examination of the lower extremities that includes inspection and assessment of fine touch, vibration sensation, and ankle reflexes. MNSI is scored by assigning points for abnormal findings. DPN was defined as present based on the following: (1) if subjects showed any abnormality in sensory and/or nerve conduction studies, and (2) if subjects had 7 or more positive responses on the MNSI questionnaire or a score of >2.0 on the MNSI examination [15]. The subjects were divided into 2 groups based on the results of their nerve conduction studies and MNSI. The subjects who were diagnosed as DPN were placed in the DPN group (n ¼ 17), and the other subjects were placed in the diabetic control (DC) group (n ¼ 25). There were no significant differences in gender, age, height, or body weight between the 2 groups. However, disease duration from diagnosis to the commencement of this study and the types of medication administered at the time of the study were significantly different between the DPN and DC groups (P ¼ .001, P ¼ .021, respectively) (Table 1).
Balance Stability Evaluation METHODS Study Subjects This study included 42 subjects with type 2 diabetes mellitus who were older than 40 years of age and were recruited from the Departments of Rehabilitation Medicine and Endocrinology at our hospital. All provided signed informed consent. Exclusion criteria were the following: a history of cardiovascular disease, orthopedic disease, renal dysfunction (serum creatinine level, 2.0 mg/dL), hepatic dysfunction (aspartate transaminase or alanine transaminase level, 40 IU/L), or other life-threatening diseases; having been medicated with gabapentin, pregabalin, or thioctic acid for pain control; and having been medicated with antipsychotic agents. Eighteen adults without diabetes, ages 40 years old or older, who met the same exclusion criteria as the subjects with diabetes were brought in as the control group (nondiabetic control [NDC] group).
Balance stability was separately assessed by using the Balance Master system after complete description of test procedures to each participant. All the participants then underwent sensory impairment assessment (SIA), tests of static balance stability and motor impairment assessment (MIA), tests of dynamic balance stability, and functional limitation assessment (FLA), as they stood in front of the monitor of the Balance Master system. Because different features of their own shoes, for example, thickness of their soles, would have influenced test results, the participants were asked to wear special shoes fitted for their feet, which were provided by the balance test laboratory (Figure 1).
SIA SIA was performed by using modified clinical test sensory interaction on balance (mCTSIB). All the subjects were asked to stand on the foam-covered force plate of the test machine,
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Table 1. General characteristics of the subjects
Total subjects, n Gender, n Men Women Mean SD age, y Mean SD height, cm Mean SD weight, kg Mean SD duration after diagnosis of DM, y Management for DM, n subjects Single oral medication 2 Kinds of oral medication 3 Kinds of oral medication Oral medication with insulin Insulin only
DPN
DC
NDC
17
25
18
8 9 60.0 11.2 161.8 8.7 69.2 9.6 8.8 5.0
13 12 55.5 8.2 160.5 7.1 65.0 9.9 4.0 3.0
7 11 52.0 6.8 159.7 6.5 60.4 8.8
1 10 0 5 1
10 10 3 2 0
DPN ¼ diabetic peripheral neuropathy; DC ¼ diabetic control; NDC ¼ nondiabetic control; SD ¼ standard deviation; DM ¼ diabetes mellitus.
and to maintain their standing posture with their eyes open for 10 seconds and again with their eyes closed for 10 seconds. Center of gravity (COG) sway velocity ( /s) was measured.
MIA MIA was performed by using the rhythmic weight shift test, a test of lefteright and fronteback COG shifts. We measured on-axis velocity and directional control according to the moving velocity (slow or fast). Slow moving was defined as 3-second transition, and fast moving was defined as 1-second transition. On-axis velocity reflects a dynamic body weight shift in an intended movement direction; the data were expressed as /s. Directional control reflects the degree of sway from a linear movement; the data were expressed as percentages.
FLA FLA was performed by using sit-to-stand, unilateral stance, tandem walk, and stepequick turn tests. In the sit-to-stand test, all the subjects were asked to place their feet on a mark on the force plate and to sit with their hip and knee joints flexed at 90 ; then they were instructed to stand while leaning their trunk forward. We measured weight transfer, rising index (the amount of force exerted by the legs during the rising phase), COG sway velocity (the control of the COG over the base of support during the rising phase and for 5 seconds thereafter), and lefteright weight symmetry (differences in weight between both legs while standing). In the unilateral stance test, all the subjects were asked to stand on 1 leg for 10 seconds on the power plate with their eyes open or closed, after which mean COG sway velocity was
Figure 1. Balance ability evaluation performed by using the Balance Master system. (A) Patients stood on the force plate for this study. (B) Sensory impairment assessment was performed by using modified clinical test sensory interaction on balance; patients stood on the foam-covered force plate. (C) Motor impairment assessment was performed by using the rhythmic weight shift. Patients tried to move the pointer to the target spot when they moved their body from left to right or from forward to backward. (D) Functional limitation assessment consisted of sit-to-stand, unilateral stance, tandem walk and stepequick turn tests.
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Table 2. Comparison of sensory impairment assessment within groups by using the mean center of gravity sway velocity ( /s)
Eye open, median (min-max) Eye closed, median (min-max)
DPN
DC
NDC
P Value
0.50 (0.3 to w1.2) 1.00 (0.6 to w1.5)
0.40 (0.2 to w0.8) 0.90 (0.6 to w1.8)
0.40 (0.2 to w0.6) 1.00 (0.4 to w1.5)
.460 .652
DPN ¼ diabetic peripheral neuropathy; DC ¼ diabetic control; NDC ¼ nondiabetic control; min ¼ minimum; max ¼ maximum.
measured. In the tandem walk test, all the subjects were asked to walk heel to toe along a central line. The measured parameters of the tandem walk test were as follows: step width (the lateral distance between the left and right feet on successive steps), walking speed, and end sway (the velocity of the anterioreposterior component of COG sway for 5 seconds beginning when the patient terminated walking). In the stepequick turn test, all the subjects were asked to take 2 steps forward, then turn 180 and return to the starting point. At that moment, we also measured their turn time (the amount of time required to execute the 180 in-place turn) and turn sway degree (the degree of body axis sway during their turn performance). For each test, 3 measurements were made, and the mean was calculated.
Statistical Analysis All statistical analyses were performed by using the SAS program (SAS Institute Inc, Cary, NC). Because the data in this study did not follow normal distribution, nonparametric tests were used. The Kruskal-Wallis test was used for comparing within 3 groups, and the Mann-Whitney U test was used for comparing between 2 groups. A P value of <.05 was considered statistically significant.
RESULTS SIA There were no significant differences in COG sway velocity with eyes open or closed among the 3 groups (Table 2).
MIA In the rhythmic weight shift test, on-axis velocity was not significantly different among the 3 groups. However, left-toright directional control in the rhythmic weight shift was significantly poorer in the DC group than in the NDC group during slow movement (P ¼ .027). During fast movement, it was poorer in the DPN group than in the NDC group (P ¼ .022) (Table 3).
FLA There were no significant differences in the results of the sit-tostand test among the 3 groups. In the unilateral stance test with both eyes open, the mean COG sway velocity was significantly higher in the DPN group than in the NDC group (P ¼ .011 for the left leg standing, P ¼ .008 for the right leg standing). When participants stood on their right leg with both eyes open, the
mean COG sway velocity was significantly higher in the DPN group than in the DC group (P ¼ .027). In the tandem walk test, walking speed was significantly lower in the DPN group than in the NDC group (P ¼ .033), and end sway was significantly greater in the DPN group than in the NDC group (P ¼ .020). There were no significant differences in stepequick turn among the 3 groups (Table 4).
DISCUSSION Balance control is affected by several factors, such as vision, proprioception, vestibular function, cerebellar function, and the muscle power of both lower extremities [16]. DPN decreases proprioception and induces numbness of the lower extremities, which leads to balance impairment [17,18]. In this study, we attempted to quantitatively evaluate balance abilities of patients with diabetes by using the Balance Master system. This instrument quantitatively assesses balance control and offers objective assessments of sensory impairment, motor impairment, and functional limitations [19]. SIA is the assessment of static balance ability when using mCTSIB. There was no difference among the 3 groups in tests in which the subjects had their eyes open or closed. However, in unilateral stance tests in the FLA, which also assesses static balance, the DPN group showed more balance instability than the NDC group when participants stood on their left leg. The DPN group also demonstrated more balance instability than both the DC and the NDC groups when participants stood on their right leg. In all cases, participants had their eyes open. It is commonly known that patients with DPN have static balance instability that is worse when visual feedback is eliminated. In this study, however, there was no difference among the 3 groups when participants performed unilateral standing with their eyes closed. Both mCTSIB and unilateral stance are static balance assessments, but unilateral stance is a more dynamic test than mCTSIB. The influence of DPN on static balance stability is minimal, and thus the mCTSIB test did not show any significant differences. However, the unilateral stance test, which is more difficult, can reveal instability. MIA is the assessment of dynamic balance ability, especially coordinated movements. In the MIA, the results of the left-to-right directional control test were significantly poorer in the DC group than in the NDC group during slow movement. During fast movement, the results were worse in the DPN group than in the NDC group. It is noteworthy that the subjects with diabetes, regardless of peripheral neuropathy, have dynamic balance instability compared with normal subjects. It is estimated that a marked decrease in directional control can increase the risk of falling and its
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Table 3. Comparison of motor impairment assessment by using the rhythmic weight shift test within groups DPN, median (min to wmax)
DC, median (min to wmax)
NDC, median (min to wmax)
3.2 (2.2 to w4.3) 78 (51 to w85)
3.1 (2.2 to w3.8) 79 (64 to w88)*
3.1 (2.5 to w4.4) 75.5 (54 to w82)*
9.6 (5.7 to w13.7) 89 (83 to w95)*
8.6 (3.0 to w13.3) 89 (77 to w95)
7.6 (3.9 to w14.8) 86.5 (78 to w92)*
2.1 (1.5 to w3.8) 76 (53 to w86)
2.1 (1.6 to w2.9) 80 (51 to w87)
2.1 (1.8 to w3.2) 80.55 (64 to w86)
5.7 (2.1 to w8.6) 83 (61 to w95)
5.1 (2.3 to w7.5) 84 (65 to w94)
5.1 (3.1 to w7.4) 85.5 (74 to w92)
Left-right Slow On-axis velocity, /s Directional control, % Fast On-axis velocity, /s Directional control, % Forward-backward Slow On-axis velocity, /s Directional control, % Fast On-axis velocity, /s Directional control, %
DPN ¼ diabetic peripheral neuropathy; min ¼ minimum; max ¼ maximum; DC ¼ diabetic control; NDC ¼ nondiabetic control. *Significant differences, P < .05.
associated injuries. In our study, we found that left-to-right sway was significantly poorer in the DPN and DC groups than in the NDC group. However, there was no significant difference in the forward-to-backward sway test. A previous study revealed postural instability in patients with DPN, especially in the mediolateral direction [10]. Furthermore, our study showed that mediolateral stability also is lower in subjects with diabetes and without neuropathy. Maki et al [20] showed that left-to-right falling increases the risk of hip joint fractures more than does forward-to-backward falling. According to the previous study and results of this study, the risk of falling may be greater in the patients with diabetes,
regardless of peripheral neuropathy, than in normal subjects. Therefore, although clinicians have focused on balance training in patients with diabetes and with peripheral neuropathy, clinicians should recognize the necessity of early balance training for the prevention of falling even in patients with diabetes and without peripheral neuropathy. In the tandem walk in the FLA, the walking speed was significantly slower and end sway was significantly greater in the DPN group than in the NDC group. In a previous study, tandem stand was worse in the diabetic groups than in the NDC group [6]. Decreased proprioception, weak muscle power, and decreased somatoreceptor function lead to
Table 4. Comparison of functional limitation assessment within groups DPN, median (min to wmax) Sit-to-stand Weight transfer, s Rising index, % COG sway velocity, /s Left-right weight symmetry, % Unilateral stance, mCOG sway velocity, /s With both eyes open Left leg standing Right leg standing With both eyes closed Left leg standing Right leg standing Tandem walk Step width, cm Walking speed, cm/s End sway, /s Stepequick turn test Left turn time, s Right turn time, s Left turn sway, degree Right turn sway, degree
0.6 19.0 2.1 8.0
(0.2 to w1.9) (11.0 to w41.0) (0.8 to w4.8) (1.0 to w22.0)
DC, median (min to wmax) 0.4 23.0 3.0 4.0
(0.3 (8.0 (0.8 (1.0
to to to to
w1.2) w48.0) w5.0) w37.0)
NDC, median (min to wmax) 0.5 24.0 2.5 6.0
(0.2 to w1.6) (15.0 to w31.0) (0.8 to w3.6) (3.0 to w24.0)
1.0 (0.4 to w4.7)* 0.9 (0.5 to w8.3)*y
0.7 (0.3 to w4.5) 0.7 (0.5 to w4.4)y
0.6 (0.3 to w1.8)* 0.7 (0.4 to w1.7)*
2.0 (0.9 to w8.4) 1.5 (1.0 to w6.7)
1.7 (1.2 to w5.1) 1.7 (1.2 to w8.7)
1.4 (0.8 to w3.2) 2.1 (0.8 to w5.2)
6.5 (4.4 to w10.2) 23.8 (16.4 to w38.4)* 4.4 (2.7 to w6.8)* 1.1 0.9 21.6 21.9
(0.5 to w2.0) (0.5 to w2.4) (15.0 to w33.7) (16.0 to w30.3)
6.3 (4.6 to w9.2) 26.4 (13.2 to w43.6) 3.9 (1.2 to w7.9) 0.7 0.8 20.0 20.0
(0.3 to w1.2) (0.3 to w1.4) (12.7 to w29.2) (9.0 to w33.1)
6.2 (4.9 to w9.5) 29.2 (20.8 to w34.3)* 3.4 (2.5 to w5.7)* 0.7 0.9 19.7 22.0
(0.3 to w1.8) (0.4 to w2.3) (9.9 to w37.5) (12.0 to w32.4)
DPN ¼ diabetic peripheral neuropathy; min ¼ minimum; max ¼ maximum; DC ¼ diabetic control; NDC ¼ nondiabetic control; COG ¼ center of gravity; mCOG ¼ mean center of gravity. *Significant differences, P < .05, comparison between DPN and NDC group. y Significant differences, P < .05, comparison between DPN and DC group.
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postural abnormalities, which increase left-to-right weight sway, decrease walking speed, and elevate step-width while walking; and, when the base of support is fixed and small, dynamic balance is worse [10]. The results of this study indicate that the absence or presence of peripheral neuropathy may affect balance control in patients with diabetes and that balance abnormalities related to specific movements can be induced in patients with diabetes and with peripheral neuropathy. In addition, we were able to quantify static, dynamic, and functional balance abnormalities. Comparative analyses of the effects of diabetes on balance stability have implications in clinical practice. Balance exercise programs are necessary for patients with diabetes to improve dynamic balance stability and to minimize the functional limitation of specific movements.
CONCLUSIONS This comparative study of balance stability between patients with diabetes and normal subjects demonstrated that balance stability related to functional limitations in specific movements decreased more significantly in patients with diabetes and with peripheral neuropathy than in patients with diabetes and without peripheral neuropathy or in normal subjects. We also found that dynamic balance control was significantly worse in patients with diabetes and without peripheral neuropathy than in normal subjects. Further studies of dynamic balance stability and functional limitation of specific movements in patients with diabetes are needed to develop balance exercise programs.
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6. Resnick HE, Stansberry KB, Harris TB, et al. Diabetes, peripheral neuropathy, and old age disability. Muscle Nerve 2002;25:43-50. 7. Strotmeyer ES, de Rekeneire N, Schwartz AV, et al. Sensory and motor peripheral nerve function and lower-extremity quadriceps strength: The health, aging and body composition study. J Am Geriatr Soc 2009; 57:2004-2010. 8. Morrison S, Colberg SR, Mariano M, Parson HK, Vinik AI. Balance training reduces falls risk in older individuals with type 2 diabetes. Diabetes Care 2010;33:748-750. 9. Morrison S, Colberg SR, Parson HK, Vinik AI. Relation between risk of falling and postural sway complexity in diabetes. Gait Posture 2012;35: 662-668. 10. Ghanavati T, Shaterzadeh Yazdi MJ, Goharpey S, Arastoo AA. Functional balance in elderly with diabetic neuropathy. Diabetes Res Clin Pract 2012;96:24-28. 11. Maurer MS, Burcham J, Cheng H. Diabetes mellitus is associated with an increased risk of falls in elderly residents of a long-term care facility. J Gerontol A Biol Sci Med Sci 2005;60:1157-1162. 12. Emam AA, Gad AM, Ahmed MM, Assal HS, Mousa SG. Quantitative assessment of posture stability using computerised dynamic posturography in type 2 diabetic patients with neuropathy and its relation to glycaemic control. Singapore Med J 2009;50:614-618. 13. Turcot K, Allet L, Golay A, Hoffmeyer P, Armand S. Investigation of standing balance in diabetic patients with and without peripheral neuropathy using accelerometers. Clin Biomech (Bristol, Avon) 2009; 24:716-721. 14. Lee H, DeLisa J. Manual of Nerve Conduction Study and Surface Anatomy for Needle Electromyography. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005. 15. Moghtaderi A, Bakhshipour A, Rashidi H. Validation of Michigan neuropathy screening instrument for diabetic peripheral neuropathy. Clin Neurol Neurosurg 2006;108:477-481. 16. Horak F. Clinical measurement of postural control in adults. Phys Ther 1987;67:1881-1885. 17. Lafond D, Corriveau H, Prince F. Postural control mechanisms during quiet standing in patients with diabetic sensory neuropathy. Diabetes Care 2004;27:173-178. 18. Akbari M, Jafari H, Moshashaee A, Forugh B. Do diabetic neuropathy patients benefit from balance training? J Rehabil Res Dev 2012;49:333-338. 19. Lim KB, Lee HJ, Joo SJ, Lim SS. Postural control measures of patients with back pain using Balance Master System. J Korean Acad Rehab Med 2007;31:30-36. 20. Maki BE, Holliday PJ, Topper AK. A prospective study of postural balance and risk of falling in an ambulatory and independent elderly population. J Gerontol 1994;49:M72-M84.
This journal-based CME activity is designated for 1.0 AMA PRA Category 1 Credit and can be completed online at www.me.aapmr.org. This activity is FREE to AAPM&R members and available to non-members for a nominal fee. For assistance with claiming CME for this activity, please contact (847) 737-6000.
CME Question Diabetics, both with and without peripheral neuropathy, were more impaired than nondiabetics in: a. b. c. d.
forward to backward sway. tandem gait walking speed. left right directional control. unilateral stance testing.
Answer online at me.aapmr.org