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Postural Control and Functional Strength in Patients With Type 2 Diabetes Mellitus With and Without Peripheral Neuropathy
Archives of Physical Medicine and Rehabilitation journal homepage: www.archives-pmr.org Archives of Physical Medicine and Rehabilitation 2013;-:-------
ORIGINAL ARTICLE
Postural Control and Functional Strength in Patients With Type 2 Diabetes Mellitus With and Without Peripheral Neuropathy Maı´ta M. Vaz, BSc,a Gustavo C. Costa, MD,a Julia G. Reis, PhD,a Wilson Marques Junior, PhD,b Francisco Jose´ Albuquerque de Paula, PhD,c Daniela C. Abreu, PhDa From the aPhysiotherapy Course, Department of Biomechanics, Medicine, and Rehabilitation of the Locomotor System, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP; bDepartment of Neuroscience and Behavioral Sciences, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP; and cDepartment of Clinical Medicine, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP, Brazil.
Abstract Objective: To assess the influence of diabetic neuropathy (DN) on balance and functional strength in patients with diabetes mellitus type 2 (DM2). Design: Cross-sectional study. Setting: Diabetes outpatient unit. Participants: Adults (NZ62; age range, 40e65y): 32 with DM2 (19 subjects without DN and 13 with DN) and 30 without DM2 (control group). Interventions: Not applicable. Main Outcome Measures: Upright balance, evaluated in 4 situations (fixed platform, unstable platform, with eyes open, with eyes closed), and functional strength, assessed with a five-times-sit-to-stand test, were analyzed using an electromagnetic system, with a sensor placed over C7 to allow maximum trunk displacements in the anterior-posterior and medial-lateral directions. The Berg Balance Scale and the Timed Up & Go test were also used. Results: Subjects with DM2 had greater anterior-posterior displacement (P<.05) in the unstable platform with eyes closed condition compared with those without DM2, whereas no difference in medial-lateral displacement was observed between these groups. A difference in time was observed in the five-times-sit-to-stand test (P<.05), with subjects in the control group performing the tasks faster than either group of subjects with DM2. Additionally, subjects in the control group showed a higher score in the Berg Balance Scale and performed the Timed Up & Go test in less time compared with subjects in other groups. Conclusions: Subjects with DM2, with or without DN, showed deficits in postural control and functional strength compared with healthy individuals of the same age group. Archives of Physical Medicine and Rehabilitation 2013;-:------ª 2013 by the American Congress of Rehabilitation Medicine
Diabetes mellitus (DM) is a growing health problem in all countries, regardless of the degree of development.1-3 The prevalence of chronic degenerative diseases has increased because of the longer life expectancy of the population in combination with a significant change in lifestyle resulting from urbanization. In addition, advances in the etiopathogenic knowledge of metabolic
Supported by the Research Foundation of Sa˜o Paulo (grant nos. 2007/54596-0; 2007/57685-4). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.
disorders have produced therapeutic alternatives for prolonging the lives of patients with degenerative diseases, thus making maintenance of their quality of life a challenge. Diabetic neuropathy (DN) is one of the most frequent complications of DM. The clinical complications resulting from DN are extremely varied, affecting both the somatic and autonomic nervous systems. In chronic sensory-motor neuropathy, the signs and symptoms vary depending on the spectrum of nerve fibers involved. Damage to large sensory fibers decreases sensitivity to light touch and position sensing, whereas damage to small fibers decreases sensitivity to pain and thermal stimuli. In general,
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both large and small fibers are involved in the neuropathic process.4 In addition to the sensory impairments resulting from neuropathy itself, individuals with diabetes mellitus type 2 (DM2) seem to be more susceptible to falls and, consequently, to fractures.5-7 Because more studies are needed to clarify the possible factors involved in the relation between postural deficits and sensorymotor neuropathy in individuals with DM2, the present study examines the influence of DN on the control of upright balance and functional strength.
Methods Thirty-two men and women with DM2 (age range, 40e65y) were evaluated; 19 subjects were without DN and 13 had DN. A subject with DN had large fiber involvement, but we did not classify the severity of the impairments. Subjects were selected by endocrinologists and neurologists from the diabetes outpatient unit of the clinical hospital and the outpatient diabetes health center unit of Ribeira˜o Preto, School of Medicine. The presence of neuropathy was investigated clinically and neurophysiologically by the neurologist. Patients were first questioned about the presence of sensory (paresthesias, dysesthesias, loss of sensation) and motor (weakness, atrophy, fatigue) symptoms. They were then given a neurologic examination that included (1) evaluation of pain, tactile, vibration, and postural sensations; (2) tests for weakness, according to the Medical Research Council,8 methodology, and atrophy; (3) tests of tendon reflexes; and (4) examination for signs of trophic abnormalities. Finally, they underwent nerve conduction studies using standard techniques.9 The sural and superficial peroneal sensory nerves and the peroneal and posterior tibial motor nerves were examined; peroneal and posterior tibial F-waves were also recorded. Latency, conduction velocity, amplitude, and morphology of the sensory and motor compound action potentials were analyzed. Nerve conduction studies were conducted using a Nihon Kohden model EP/EMG system.a We noted the presence of abnormal vibratory and proprioception sensations, distal weakness and atrophy, and decreased or absent tendon jerks, which are also the result of large fiber neuropathology. A third group of individuals without DM2 (control group) was matched by age, weight, and height with the subjects with DM2 for purposes of comparison (fig 1). To ensure that this study was conducted in accordance with relevant ethical principles, each participant signed an institutional informed consent document that had been approved by the institution’s ethics committee (Clinicas Hospital of Ribeira˜o Preto no.
List of abbreviations: AP BBS DM DM2 DN FPEC FPEO FTSST ICC ML TUG UPEC UPEO
anterior-posterior Berg Balance Scale diabetes mellitus diabetes mellitus type 2 diabetic neuropathy fixed platform with eyes closed fixed platform with eyes open five-times-sit-to-stand test intraclass correlation coefficient medial-lateral Timed Up & Go unstable platform with eyes closed unstable platform with eyes open
1500/2008). The data were collected at the Laboratory of Assessment and Rehabilitation of Equilibrium at the Clinical Hospital of the Ribeira˜o Preto, School of Medicine. The exclusion criteria were the following: diagnosis of cardiovascular, neurologic, rheumatologic, or musculoskeletal diseases that might interfere with daily life activities; use of drugs that potentially have negative effects on cognition, alertness, and psychomotor function (ie, opioids, antiepileptics, anxiolytics, antipsychotics, hypnotics, sedatives); the presence of vestibulopathies; and injuries in the lower limbs or a history of fracture in the last 6 months. On the day of assessment, the subjects were asked about falls in the last 12 months, and the weight and height of each subject were measured. To evaluate balance and functional strength, a Polhemus device (3SPACE Isotrak II)b with 2 sensors emitting and detecting magnetic fields was used. One of the sensors was placed over C7, and the transmitter coil was placed at a distance of 60cm from the subjects.10,11 By means of signals obtained from the sensors, deviations in the x (anterior-posterior [AP]), y (medial-lateral [ML]), and z (vertical) planes can be measured.10-14 The Polhemus device precisely measures all trunk movements through its transmitter coil, which emits an electromagnetic field that is detected by the sensor. The device was calibrated before each evaluation by placing the transmitter coil on a hard level surface, shifting it forward 2cm, and assessing the accuracy of the system in measuring the displacement. Prior to beginning the evaluation of upright balance, the subjects remained seated at rest for 5 minutes. During the tests, they were in a standing position, barefoot, and had their shoulders and feet aligned and arms parallel to the femoral heads. Starting in this posture, the test was performed in the following 4 situations: (1) standing on a wooden fixed platform with eyes open (FPEO) for 60 seconds; (2) standing on a wooden fixed platform with eyes closed (FPEC) for 60 seconds; (3) standing on a table platform (foam, 5-cm thickness and density of 30g/dm3) with eyes open (UPEO) for 60 seconds; and (4) standing on a foam platform (5-cm thickness and density of 30g/dm3) with eyes closed (UPEC) for 60 seconds. During the upright balance test with eyes open, there was a fixed point at a distance of 150cm from the subjects. The maximum trunk displacements in the AP and ML directions were evaluated in the 4 situations. Functional strength was evaluated using the five-times-sit-tostand test (FTSST). The subjects were seated on a chair with their hips and knees flexed at 90 (measured with a goniometer). The subjects were instructed to keep their arms crossed over their trunk with the palms of the hands facing toward the chest while looking ahead. On hearing a verbal command, the subjects had to stand up and sit down 5 times consecutively as quickly as possible. The Polhemus device’s sensor was placed over C7. The time needed to perform the FTSST and the AP displacement of the trunk during the 5 repetitions were measured, and a mean value was obtained. This test is usually performed to evaluate the balance and strength of the lower limbs.11,15,16 In order to identify the inter- and intrarater reliability for the Polhemus device, a pilot study was performed and the obtained results are presented. The intrarater reliability results were obtained for the FTSST (rise: intraclass correlation coefficient (ICC) Z.98, descent: ICCZ.99, time: ICCZ.99) and the balance tests (FPEO: ICCZ.96, FPEC: ICCZ.99, UPEO: ICCZ.83, UPEC: ICCZ.95). The interrater reliability results for the FTSST (rise: www.archives-pmr.org
Balance evaluation and type 2 diabetes
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Fig 1
Flow diagram for group assignment.
ICCZ.91, descent: ICCZ.87, time: ICCZ.95) and the balance tests (FPEO: ICCZ.98, FPEC: ICCZ.82, UPEO: ICCZ.89, UPEC: ICCZ.99) were also obtained. The Berg Balance Scale (BBS)17 was used to assess functional balance performance based on 14 daily life related items. The maximum score is 56, and each item has a 5-point scale ranging from 0 to 4. The test is simple, safe, and easy to apply in clinical practice.18 Based on Shumway-Cook et al,19 in the range of 56 to 54, each 1-point drop in the BBS is related to a 3% to 4% risk of falling increase. In the range of 54 to 46, each 1-point drop refers to an increase of 6% to 8% for the risk of falling, and <36 points the risk of falls is close 100%. Therefore, a change of 1 point in the BBS can result in very different percentages because it depends on the total score and, consequently, represents a different risk of falls. To test functional mobility, the Timed Up & Go (TUG) test was used. The subjects had to stand up, walk 3m, return to the chair, and sit down,20 all at their regular pace after the verbal command “go.” The stopwatch started after the verbal command and stopped when the subjects were seated again with their back resting on the back of the chair. The chair had a backrest and armrests with the height adjusted; therefore, the subjects’ knees www.archives-pmr.org
could be flexed at an angle of 90 with the feet flat on the floor. The test was performed twice, with the first attempt for familiarization and the second attempt for recording the time. Many studies have already shown high intrarater and interrater reliability for the BBS17,18 and TUG test.20,21 The Shapiro-Wilk test and Levene tests were used to assess the normality and homogeneity of the variables studied, respectively. When necessary, the variables were transformed until a normative distribution was achieved. For data analysis, an analysis of variance was performed 16 times, and the post hoc Tukey test was applied when necessary. All analyses were performed using SPSS softwarec at a significance level of P<.05.
Results No differences between groups were found regarding age (F2.57Z.21, P>.05), weight (F2.57Z.77, P>.05), and height (F2.57Z.50, P>.05). Subjects with DM2 and DN had DM for a longer time (they have been living with the disease for more years) than those without neuropathy (F1.28Z4.57, P<.05).
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Among the subjects with DM2, 57.9% of subjects without DN and 84.6% with neuropathy reported the occurrence of falls in the last year. Differences between groups of individuals with and without DM2 were observed using the BBS (F2.57Z12.98, P<.05) and TUG test (F2.57Z21.25, P<.05). Individuals in the control group showed better results compared with individuals with and without DM. Table 1 lists the general characteristics of the subjects included in the study and the results of the clinical tests. The evaluation of upright balance in the 4 experimental situations (FPEO, FPEC, UPEO, and UPEC) showed a difference in AP displacement only in the UPEC situation (F2.57Z5.86, P<.05), and the subjects with and without neuropathy showed greater trunk displacement compared with the controls. However, no difference between the groups was observed in terms of ML displacement. Figure 2 shows the mean values for the maximum AP and ML displacements of the trunk, respectively. The results of the FTSST did not show a difference between groups in terms of AP displacement, although a difference was observed in the time spent to perform the FTSST (F2.57Z17.25, P<.05), with the subjects in the control group performing the FTSST in less time than subjects with DM2 or without neuropathy. Table 2 shows the mean values of the maximum trunk displacement for the FTSST and the total time spent to perform the FTSST in all groups.
Discussion The duration of DM2 has been associated with an increased prevalence of diabetic complications, such as diabetic retinopathy22 and DN.23 Decreases in neural sensitivity, muscle strength, and muscle reflexes can significantly impair the balance of patients and predispose them to falls. In addition, there seems to be a relation between subjects with DM2 and a higher risk of falls and fractures.24 Therefore, because of the importance of the sensory information available from vestibular, visual, and somatosensory systems for postural control, assessing the upright balance of people with DM2 is important. The presence of DN should be assessed to analyze the contribution of different sensory systems to the maintenance of balance in this condition. Moreover, the evaluation of these skills during functional activities provides further information about the capacity of patients to integrate postural control, coordination, muscle strength, and mobility, which allows for the determination of whether peripheral neuropathy interferes with these motor activities. TUG is a balance test that is commonly used to examine functional mobility, and the time required to perform the test is strongly related to the risk of falls. Healthy adults can perform the test in a maximum of 10 seconds, and this value predicts a lesser Table 1 Groups
risk of falls.20 Although there was a statistically significant difference between the groups with and without DM2, this difference was not clinically meaningful because the times required for all groups were <10 seconds, which is associated with adequate functional mobility. However, based on the study of Isles et al,25 the values obtained in the present study for individuals in both groups with DM2 are the values expected for older adults (60e88y). Therefore, individuals with DM2 seem to present some degree of impairment in the proactive aspect of postural control, which interferes with their functional mobility.26 The impairment of mobility was also reported by Saely et al,27 who observed that subjects with DM2 had a greater deficit in mobility compared with individuals without DM2 (40.2% vs 22.0%; P<.001). The BBS showed that the subjects with DM2 had lower scores than the controls (P<.05), with no significant difference between the subjects with and without neuropathy. Our findings are similar to those of Fulk et al,28 who reported differences only between individuals with and without DM2 and not between individuals with and without DN. Many studies29,30 have used a BBS score of 45 as the clinical cutoff to determine a risk of falls. Other studies17,19,26 have used the obtained score to establish the percentage of risk of falling because a 1-point difference in the BBS score, related to the total score, differently predicts the risk of falling. The results of the present study using the BBS show that the group of individuals without peripheral neuropathy had an increased risk of falling of 30% to 40%, whereas individuals with peripheral neuropathy had an increase ranging from 42% to 56%, demonstrating that the presence of peripheral neuropathy can impair balance in adults and the increase of risk of falls probably is associated with the severity of proprioceptive damages, which can be in larger or smaller proportions. Despite these calculations, the self-reported history of falls obtained from the individuals with DM2 was even higher (57.9% without DN and 84.6% with DN) than the BBS values. According to Cordeiro et al,31 the impaired balance and mobility observed in older adult outpatients with DM are mainly related to advanced age, limitations in the performance of daily activities, the absence of a balance strategy, and poor somatosensory sensitivity.31 Thus, we can assume that the aging process in the patients with DM2, who also had peripheral neuropathy, can cause even more impairment in balance performance. Previous studies demonstrated32,33 that the reduction of sensory information, such as visual, somatosensory, or vestibular inputs, causes instability in the body. The isolated use of the vestibular system (a challenging somatosensory environmentdthe UPEC situation) for the maintenance of balance displays the greatest postural instability,32 thus corroborating our findings. Additionally, it was observed that the subjects with DM2 had an AP displacement of the trunk during UPEC greater than that of the
General characteristics of subjects included in the study and results of clinical trials performed n
Sex (M/W) Age (y)
DM2 without peripheral neuropathy 19 3/17 DM2 with peripheral neuropathy 13 6/7 Control 30 10/20
Weight (kg) Height (cm)
53.87.7 75.416.6 54.65.5 74.610.7 54.15.7 70.611.4
Diagnosis Time (y) BBS (score) TUG (s)
160.16.7 11.65.8 163.06.0 17.28.5 160.8160.8 NA
50.36.3* 48.67.2* 55.60.8
8.41.6* 8.61.8* 6.40.5
NOTE. Data are presented as mean SD. Abbreviations: Diagnosis time, length of time with diabetes; M, men; NA, not applicable; W, women. * P<.05 compared with controls.
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Fig 2 Values of the maximum AP (A) and ML (B) displacements of the trunk during the upright balance assessment in all groups evaluated. The data are presented as mean SD. *P<.05 compared with controls.
controls (P<.05), although the presence of DN did not contribute to impaired trunk oscillation. Therefore, a dark environment with an irregular support surface is a situation in which the risk of falling increases in this population. Considering that older adults were less stable than young adults when they were exposed to visual privation,34 it is expected that the aging process would have a worse impact on individuals with DM2. The FTSST was used to assess functional muscle strength and postural control and mobility; it is easy to use and allows for the identification of individuals with poor balance. In the FTSST, the subjects with DM2 took more time to complete the test compared with the controls, suggesting that the former have a higher risk of falls during dynamic situations in which integration of several body components, such as the sensory system, motor coordination, mobility, and muscle strength, are required.35 Individuals with DM2 but without DN performed the FTSST in 14.93.5 seconds, and those with DN performed the test in 15.12.7 seconds. These values are similar to those determined by Ribeiro et al36 for women with and without a history of falls and with a mean age of 70.66.8 and 68.54.2 years, respectively. On the other hand, the values obtained in the present study are higher than those obtained by Bohannon16 for older adults between 80 and 89 years of age. However, in the present study, there was no difference in the AP trunk displacement during the FTSST among the groups. To our knowledge, no study has assessed trunk displacement during the FTSST in individuals with DM2 with or without DN. However, Trevisan et al11 showed AP displacement of the trunk in a population of women with osteoporosis during the FTSST, suggesting that a greater AP trunk displacement was related to compensation strategies during the test, relating to impaired motor skills that caused them to be more susceptible to falls.
The results show that the individuals with DM2 had an impairment of postural control compared with the individuals without DM2 in both the upright position and in dynamic situations, but individuals in the DN group had no more impairment of postural control in the variables studied than other subjects with DM2. A BBS score of 45 was considered the cutoff to determine risk of falling, and a TUG test time >10 seconds was used to determine mobility impairment; it is important to emphasize that the results obtained in the present study using these criteria do not reflect the higher percentage of falls actually reported by subjects in the group with DM2. Moreover, it was only possible to observe a higher risk of falls in the presence of neuropathy when percentage values were considered in the classification for the BBS, suggested by Berg et al,17 rather than by using the cutoff score. Proprioceptive pathways consist of large nerve fibers, and all patients included in the group with DN exhibited involvement of these fibers.4,37 However, the severity of proprioceptive impairment of the subjects in this group was not taken into account, a fact that may have contributed to the similarity in balance performance in the groups without and with neuropathy.
Study limitations The main limitation of this study was the variation in the severity of distal sensory large fiber polyneuropathy in the group of individuals with DN. Because there are few studies that evaluated the balance aspects in subjects with DM, it should be emphasized that our findings contribute to a better understanding of the changes in balance and functional mobility in individuals with DM2.
Conclusions Table 2 Maximum values for maximum AP displacement of the trunk during the FTSST and the time spent to perform the FTSST in all groups Groups
Rise (cm) Descent (cm) Time Spent (s)
DM2 without peripheral 13.64.1 14.83.4 neuropathy DM2 with peripheral 15.34.3 15.93.6 neuropathy Control 12.16.4 12.36.4 NOTE. Data are presented as mean SD. * P<.05 compared with controls.
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Individuals with DM2, compared with controls, have impaired postural control and functional strength. With regard to the variables studied, no difference was observed between individuals with DM2 and without distal neuropathy.
14.93.5* 15.12.7* 10.62.4
Suppliers a. MEB-9200J; Nihon Kohden, Tokyo, Japan. b. 3SPACE and Isotrak II; Polhemus, 40 Hercules Dr, Colchester, VT 05446. c. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
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Keywords Diabetic neuropathies; Rehabilitation
Corresponding author Prof. Dra. Daniela Cristina Carvalho de Abreu, PhD, Avenida Bandeirantes, 3900, Ribeira˜o Preto, SP, Brasil, CEP: 14049-900. E-mail address: [email protected].
Acknowledgments We thank the Bioengineering Unit (School of Medicine of University of Sa˜o Paulo-Ribeira˜o Preto) for the support provided.
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M.M. Vaz et al 16. Bohannon RW. Reference values for the five-repetition sit-to-stand test: a descriptive meta-analysis of data from elders. Percept Motor Skills 2006;103:215-22. 17. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: validation of an instrument. Can J Public Health 1992;83(Suppl 2):S7-11. 18. Miyamoto ST, Lombardi Junior I, Berg KO, Ramos LR, Natour J. Brazilian version of the Berg balance scale. Braz J Med Biol Res 2004;37:1411-21. 19. Shumway-Cook A, Baldwin M, Polissar NL, Gruber W. Predicting the probability for falls in community-dwelling older adults. Phys Ther 1997;77:812-9. 20. Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991;39:142-8. 21. Shumway-Cook A, Brauer S, Woollacott M. Predicting the probability for falls in community-dwelling older adults using the Timed Up & Go Test. Phys Ther 2000;80:896-903. 22. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy. III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol 1984;102:527-32. 23. Young MJ, Boulton AJ, MacLeod AF, Williams DR, Sonksen PH. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993;36:150-4. 24. Bruce DG. Type 2 diabetes mellitus and disability. In: Stone JH, Blouin M, editors. International encyclopedia of rehabilitation. Sa˜o Carlos (Brazil): Rev Bras Fisioter; 2012. 25. Isles RC, Choy NL, Steer M, Nitz JC. Normal values of balance tests in women aged 20-80. J Am Geriatr Soc 2004;52:1367-72. 26. Shumway-Cook A, Woollacott MH. Motor control: translating research into clinical practice. 4th ed. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2012. 27. Saely CH, Dyballa T, Vonbank A, et al. Type 2 diabetes but not coronary atherosclerosis is an independent determinant of impaired mobility in angiographied coronary patients. Diabetes Res Clin Pract 2008;82:185-9. 28. Fulk GD, Robinson CJ, Mondal S, Storey CM, Hollister AM. The effects of diabetes and/or peripheral neuropathy in detecting short postural perturbations in mature adults. J Neuroeng Rehabil 2010;7:44. 29. Swanenburg J, de Bruin ED, Stauffacher M, Mulder T, Uebelhart D. Effects of exercise and nutrition on postural balance and risk of falling in elderly people with decreased bone mineral density: randomized controlled trial pilot study. Clin Rehabil 2007;21:523-34. 30. Madureira MM, Takayama L, Gallinaro AL, Caparbo VF, Costa RA, Pereira RM. Balance training program is highly effective in improving functional status and reducing the risk of falls in elderly women with osteoporosis: a randomized controlled trial. Osteoporos Int 2007;18:419-25. 31. Cordeiro RC, Jardim JR, Perracini MR, Ramos LR. Factors associated with functional balance and mobility among elderly diabetic outpatients. Arq Bras Endocrinol Metabol 2009;53:834-43. 32. Horak FB. Postural orientation and equilibrium: what do we need to know about neural control of balance to prevent falls? Age Ageing 2006;35(Suppl 2):ii7-11. 33. Manchester D, Woollacott M, Zederbauer-Hylton N, Marin O. Visual, vestibular and somatosensory contributions to balance control in the older adult. J Gerontol 1989;44:M118-27. 34. Hay L, Bard C, Fleury M, Teasdale N. Availability of visual and proprioceptive afferent messages and postural control in elderly adults. Exp Brain Res 1996;108:129-39. 35. Karinkanta S, Heinonen A, Sievanen H, Uusi-Rasi K, Kannus P. Factors predicting dynamic balance and quality of life in homedwelling elderly women. Gerontology 2005;51:116-21. 36. Ribeiro AMP, Gomes MM, Rosa RC, Abreu DCC. Is the history of falls an indicative of greater decline in quadriceps muscle function and postural sway? Top Geriatr Rehabil 2012;28:60-6. 37. Gadsby R. The diabetic foot in primary care: a UK perspective. In: Connor H, Cavanagh PR, editors. The foot in diabetes. Chichester (UK): John Wiley & Sons, Ltd; 2000. p 95-103.
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ORIGINAL ARTICLE
Postural Control and Functional Strength in Patients With Type 2 Diabetes Mellitus With and Without Peripheral Neuropathy Maı´ta M. Vaz, BSc,a Gustavo C. Costa, MD,a Julia G. Reis, PhD,a Wilson Marques Junior, PhD,b Francisco Jose´ Albuquerque de Paula, PhD,c Daniela C. Abreu, PhDa From the aPhysiotherapy Course, Department of Biomechanics, Medicine, and Rehabilitation of the Locomotor System, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP; bDepartment of Neuroscience and Behavioral Sciences, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP; and cDepartment of Clinical Medicine, University of Sa˜o Paulo, School of Medicine, Ribeira˜o Preto, SP, Brazil.
Abstract Objective: To assess the influence of diabetic neuropathy (DN) on balance and functional strength in patients with diabetes mellitus type 2 (DM2). Design: Cross-sectional study. Setting: Diabetes outpatient unit. Participants: Adults (NZ62; age range, 40e65y): 32 with DM2 (19 subjects without DN and 13 with DN) and 30 without DM2 (control group). Interventions: Not applicable. Main Outcome Measures: Upright balance, evaluated in 4 situations (fixed platform, unstable platform, with eyes open, with eyes closed), and functional strength, assessed with a five-times-sit-to-stand test, were analyzed using an electromagnetic system, with a sensor placed over C7 to allow maximum trunk displacements in the anterior-posterior and medial-lateral directions. The Berg Balance Scale and the Timed Up & Go test were also used. Results: Subjects with DM2 had greater anterior-posterior displacement (P<.05) in the unstable platform with eyes closed condition compared with those without DM2, whereas no difference in medial-lateral displacement was observed between these groups. A difference in time was observed in the five-times-sit-to-stand test (P<.05), with subjects in the control group performing the tasks faster than either group of subjects with DM2. Additionally, subjects in the control group showed a higher score in the Berg Balance Scale and performed the Timed Up & Go test in less time compared with subjects in other groups. Conclusions: Subjects with DM2, with or without DN, showed deficits in postural control and functional strength compared with healthy individuals of the same age group. Archives of Physical Medicine and Rehabilitation 2013;-:------ª 2013 by the American Congress of Rehabilitation Medicine
Diabetes mellitus (DM) is a growing health problem in all countries, regardless of the degree of development.1-3 The prevalence of chronic degenerative diseases has increased because of the longer life expectancy of the population in combination with a significant change in lifestyle resulting from urbanization. In addition, advances in the etiopathogenic knowledge of metabolic
Supported by the Research Foundation of Sa˜o Paulo (grant nos. 2007/54596-0; 2007/57685-4). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.
disorders have produced therapeutic alternatives for prolonging the lives of patients with degenerative diseases, thus making maintenance of their quality of life a challenge. Diabetic neuropathy (DN) is one of the most frequent complications of DM. The clinical complications resulting from DN are extremely varied, affecting both the somatic and autonomic nervous systems. In chronic sensory-motor neuropathy, the signs and symptoms vary depending on the spectrum of nerve fibers involved. Damage to large sensory fibers decreases sensitivity to light touch and position sensing, whereas damage to small fibers decreases sensitivity to pain and thermal stimuli. In general,
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both large and small fibers are involved in the neuropathic process.4 In addition to the sensory impairments resulting from neuropathy itself, individuals with diabetes mellitus type 2 (DM2) seem to be more susceptible to falls and, consequently, to fractures.5-7 Because more studies are needed to clarify the possible factors involved in the relation between postural deficits and sensorymotor neuropathy in individuals with DM2, the present study examines the influence of DN on the control of upright balance and functional strength.
Methods Thirty-two men and women with DM2 (age range, 40e65y) were evaluated; 19 subjects were without DN and 13 had DN. A subject with DN had large fiber involvement, but we did not classify the severity of the impairments. Subjects were selected by endocrinologists and neurologists from the diabetes outpatient unit of the clinical hospital and the outpatient diabetes health center unit of Ribeira˜o Preto, School of Medicine. The presence of neuropathy was investigated clinically and neurophysiologically by the neurologist. Patients were first questioned about the presence of sensory (paresthesias, dysesthesias, loss of sensation) and motor (weakness, atrophy, fatigue) symptoms. They were then given a neurologic examination that included (1) evaluation of pain, tactile, vibration, and postural sensations; (2) tests for weakness, according to the Medical Research Council,8 methodology, and atrophy; (3) tests of tendon reflexes; and (4) examination for signs of trophic abnormalities. Finally, they underwent nerve conduction studies using standard techniques.9 The sural and superficial peroneal sensory nerves and the peroneal and posterior tibial motor nerves were examined; peroneal and posterior tibial F-waves were also recorded. Latency, conduction velocity, amplitude, and morphology of the sensory and motor compound action potentials were analyzed. Nerve conduction studies were conducted using a Nihon Kohden model EP/EMG system.a We noted the presence of abnormal vibratory and proprioception sensations, distal weakness and atrophy, and decreased or absent tendon jerks, which are also the result of large fiber neuropathology. A third group of individuals without DM2 (control group) was matched by age, weight, and height with the subjects with DM2 for purposes of comparison (fig 1). To ensure that this study was conducted in accordance with relevant ethical principles, each participant signed an institutional informed consent document that had been approved by the institution’s ethics committee (Clinicas Hospital of Ribeira˜o Preto no.
List of abbreviations: AP BBS DM DM2 DN FPEC FPEO FTSST ICC ML TUG UPEC UPEO
anterior-posterior Berg Balance Scale diabetes mellitus diabetes mellitus type 2 diabetic neuropathy fixed platform with eyes closed fixed platform with eyes open five-times-sit-to-stand test intraclass correlation coefficient medial-lateral Timed Up & Go unstable platform with eyes closed unstable platform with eyes open
1500/2008). The data were collected at the Laboratory of Assessment and Rehabilitation of Equilibrium at the Clinical Hospital of the Ribeira˜o Preto, School of Medicine. The exclusion criteria were the following: diagnosis of cardiovascular, neurologic, rheumatologic, or musculoskeletal diseases that might interfere with daily life activities; use of drugs that potentially have negative effects on cognition, alertness, and psychomotor function (ie, opioids, antiepileptics, anxiolytics, antipsychotics, hypnotics, sedatives); the presence of vestibulopathies; and injuries in the lower limbs or a history of fracture in the last 6 months. On the day of assessment, the subjects were asked about falls in the last 12 months, and the weight and height of each subject were measured. To evaluate balance and functional strength, a Polhemus device (3SPACE Isotrak II)b with 2 sensors emitting and detecting magnetic fields was used. One of the sensors was placed over C7, and the transmitter coil was placed at a distance of 60cm from the subjects.10,11 By means of signals obtained from the sensors, deviations in the x (anterior-posterior [AP]), y (medial-lateral [ML]), and z (vertical) planes can be measured.10-14 The Polhemus device precisely measures all trunk movements through its transmitter coil, which emits an electromagnetic field that is detected by the sensor. The device was calibrated before each evaluation by placing the transmitter coil on a hard level surface, shifting it forward 2cm, and assessing the accuracy of the system in measuring the displacement. Prior to beginning the evaluation of upright balance, the subjects remained seated at rest for 5 minutes. During the tests, they were in a standing position, barefoot, and had their shoulders and feet aligned and arms parallel to the femoral heads. Starting in this posture, the test was performed in the following 4 situations: (1) standing on a wooden fixed platform with eyes open (FPEO) for 60 seconds; (2) standing on a wooden fixed platform with eyes closed (FPEC) for 60 seconds; (3) standing on a table platform (foam, 5-cm thickness and density of 30g/dm3) with eyes open (UPEO) for 60 seconds; and (4) standing on a foam platform (5-cm thickness and density of 30g/dm3) with eyes closed (UPEC) for 60 seconds. During the upright balance test with eyes open, there was a fixed point at a distance of 150cm from the subjects. The maximum trunk displacements in the AP and ML directions were evaluated in the 4 situations. Functional strength was evaluated using the five-times-sit-tostand test (FTSST). The subjects were seated on a chair with their hips and knees flexed at 90 (measured with a goniometer). The subjects were instructed to keep their arms crossed over their trunk with the palms of the hands facing toward the chest while looking ahead. On hearing a verbal command, the subjects had to stand up and sit down 5 times consecutively as quickly as possible. The Polhemus device’s sensor was placed over C7. The time needed to perform the FTSST and the AP displacement of the trunk during the 5 repetitions were measured, and a mean value was obtained. This test is usually performed to evaluate the balance and strength of the lower limbs.11,15,16 In order to identify the inter- and intrarater reliability for the Polhemus device, a pilot study was performed and the obtained results are presented. The intrarater reliability results were obtained for the FTSST (rise: intraclass correlation coefficient (ICC) Z.98, descent: ICCZ.99, time: ICCZ.99) and the balance tests (FPEO: ICCZ.96, FPEC: ICCZ.99, UPEO: ICCZ.83, UPEC: ICCZ.95). The interrater reliability results for the FTSST (rise: www.archives-pmr.org
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Fig 1
Flow diagram for group assignment.
ICCZ.91, descent: ICCZ.87, time: ICCZ.95) and the balance tests (FPEO: ICCZ.98, FPEC: ICCZ.82, UPEO: ICCZ.89, UPEC: ICCZ.99) were also obtained. The Berg Balance Scale (BBS)17 was used to assess functional balance performance based on 14 daily life related items. The maximum score is 56, and each item has a 5-point scale ranging from 0 to 4. The test is simple, safe, and easy to apply in clinical practice.18 Based on Shumway-Cook et al,19 in the range of 56 to 54, each 1-point drop in the BBS is related to a 3% to 4% risk of falling increase. In the range of 54 to 46, each 1-point drop refers to an increase of 6% to 8% for the risk of falling, and <36 points the risk of falls is close 100%. Therefore, a change of 1 point in the BBS can result in very different percentages because it depends on the total score and, consequently, represents a different risk of falls. To test functional mobility, the Timed Up & Go (TUG) test was used. The subjects had to stand up, walk 3m, return to the chair, and sit down,20 all at their regular pace after the verbal command “go.” The stopwatch started after the verbal command and stopped when the subjects were seated again with their back resting on the back of the chair. The chair had a backrest and armrests with the height adjusted; therefore, the subjects’ knees www.archives-pmr.org
could be flexed at an angle of 90 with the feet flat on the floor. The test was performed twice, with the first attempt for familiarization and the second attempt for recording the time. Many studies have already shown high intrarater and interrater reliability for the BBS17,18 and TUG test.20,21 The Shapiro-Wilk test and Levene tests were used to assess the normality and homogeneity of the variables studied, respectively. When necessary, the variables were transformed until a normative distribution was achieved. For data analysis, an analysis of variance was performed 16 times, and the post hoc Tukey test was applied when necessary. All analyses were performed using SPSS softwarec at a significance level of P<.05.
Results No differences between groups were found regarding age (F2.57Z.21, P>.05), weight (F2.57Z.77, P>.05), and height (F2.57Z.50, P>.05). Subjects with DM2 and DN had DM for a longer time (they have been living with the disease for more years) than those without neuropathy (F1.28Z4.57, P<.05).
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Among the subjects with DM2, 57.9% of subjects without DN and 84.6% with neuropathy reported the occurrence of falls in the last year. Differences between groups of individuals with and without DM2 were observed using the BBS (F2.57Z12.98, P<.05) and TUG test (F2.57Z21.25, P<.05). Individuals in the control group showed better results compared with individuals with and without DM. Table 1 lists the general characteristics of the subjects included in the study and the results of the clinical tests. The evaluation of upright balance in the 4 experimental situations (FPEO, FPEC, UPEO, and UPEC) showed a difference in AP displacement only in the UPEC situation (F2.57Z5.86, P<.05), and the subjects with and without neuropathy showed greater trunk displacement compared with the controls. However, no difference between the groups was observed in terms of ML displacement. Figure 2 shows the mean values for the maximum AP and ML displacements of the trunk, respectively. The results of the FTSST did not show a difference between groups in terms of AP displacement, although a difference was observed in the time spent to perform the FTSST (F2.57Z17.25, P<.05), with the subjects in the control group performing the FTSST in less time than subjects with DM2 or without neuropathy. Table 2 shows the mean values of the maximum trunk displacement for the FTSST and the total time spent to perform the FTSST in all groups.
Discussion The duration of DM2 has been associated with an increased prevalence of diabetic complications, such as diabetic retinopathy22 and DN.23 Decreases in neural sensitivity, muscle strength, and muscle reflexes can significantly impair the balance of patients and predispose them to falls. In addition, there seems to be a relation between subjects with DM2 and a higher risk of falls and fractures.24 Therefore, because of the importance of the sensory information available from vestibular, visual, and somatosensory systems for postural control, assessing the upright balance of people with DM2 is important. The presence of DN should be assessed to analyze the contribution of different sensory systems to the maintenance of balance in this condition. Moreover, the evaluation of these skills during functional activities provides further information about the capacity of patients to integrate postural control, coordination, muscle strength, and mobility, which allows for the determination of whether peripheral neuropathy interferes with these motor activities. TUG is a balance test that is commonly used to examine functional mobility, and the time required to perform the test is strongly related to the risk of falls. Healthy adults can perform the test in a maximum of 10 seconds, and this value predicts a lesser Table 1 Groups
risk of falls.20 Although there was a statistically significant difference between the groups with and without DM2, this difference was not clinically meaningful because the times required for all groups were <10 seconds, which is associated with adequate functional mobility. However, based on the study of Isles et al,25 the values obtained in the present study for individuals in both groups with DM2 are the values expected for older adults (60e88y). Therefore, individuals with DM2 seem to present some degree of impairment in the proactive aspect of postural control, which interferes with their functional mobility.26 The impairment of mobility was also reported by Saely et al,27 who observed that subjects with DM2 had a greater deficit in mobility compared with individuals without DM2 (40.2% vs 22.0%; P<.001). The BBS showed that the subjects with DM2 had lower scores than the controls (P<.05), with no significant difference between the subjects with and without neuropathy. Our findings are similar to those of Fulk et al,28 who reported differences only between individuals with and without DM2 and not between individuals with and without DN. Many studies29,30 have used a BBS score of 45 as the clinical cutoff to determine a risk of falls. Other studies17,19,26 have used the obtained score to establish the percentage of risk of falling because a 1-point difference in the BBS score, related to the total score, differently predicts the risk of falling. The results of the present study using the BBS show that the group of individuals without peripheral neuropathy had an increased risk of falling of 30% to 40%, whereas individuals with peripheral neuropathy had an increase ranging from 42% to 56%, demonstrating that the presence of peripheral neuropathy can impair balance in adults and the increase of risk of falls probably is associated with the severity of proprioceptive damages, which can be in larger or smaller proportions. Despite these calculations, the self-reported history of falls obtained from the individuals with DM2 was even higher (57.9% without DN and 84.6% with DN) than the BBS values. According to Cordeiro et al,31 the impaired balance and mobility observed in older adult outpatients with DM are mainly related to advanced age, limitations in the performance of daily activities, the absence of a balance strategy, and poor somatosensory sensitivity.31 Thus, we can assume that the aging process in the patients with DM2, who also had peripheral neuropathy, can cause even more impairment in balance performance. Previous studies demonstrated32,33 that the reduction of sensory information, such as visual, somatosensory, or vestibular inputs, causes instability in the body. The isolated use of the vestibular system (a challenging somatosensory environmentdthe UPEC situation) for the maintenance of balance displays the greatest postural instability,32 thus corroborating our findings. Additionally, it was observed that the subjects with DM2 had an AP displacement of the trunk during UPEC greater than that of the
General characteristics of subjects included in the study and results of clinical trials performed n
Sex (M/W) Age (y)
DM2 without peripheral neuropathy 19 3/17 DM2 with peripheral neuropathy 13 6/7 Control 30 10/20
Weight (kg) Height (cm)
53.87.7 75.416.6 54.65.5 74.610.7 54.15.7 70.611.4
Diagnosis Time (y) BBS (score) TUG (s)
160.16.7 11.65.8 163.06.0 17.28.5 160.8160.8 NA
50.36.3* 48.67.2* 55.60.8
8.41.6* 8.61.8* 6.40.5
NOTE. Data are presented as mean SD. Abbreviations: Diagnosis time, length of time with diabetes; M, men; NA, not applicable; W, women. * P<.05 compared with controls.
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Fig 2 Values of the maximum AP (A) and ML (B) displacements of the trunk during the upright balance assessment in all groups evaluated. The data are presented as mean SD. *P<.05 compared with controls.
controls (P<.05), although the presence of DN did not contribute to impaired trunk oscillation. Therefore, a dark environment with an irregular support surface is a situation in which the risk of falling increases in this population. Considering that older adults were less stable than young adults when they were exposed to visual privation,34 it is expected that the aging process would have a worse impact on individuals with DM2. The FTSST was used to assess functional muscle strength and postural control and mobility; it is easy to use and allows for the identification of individuals with poor balance. In the FTSST, the subjects with DM2 took more time to complete the test compared with the controls, suggesting that the former have a higher risk of falls during dynamic situations in which integration of several body components, such as the sensory system, motor coordination, mobility, and muscle strength, are required.35 Individuals with DM2 but without DN performed the FTSST in 14.93.5 seconds, and those with DN performed the test in 15.12.7 seconds. These values are similar to those determined by Ribeiro et al36 for women with and without a history of falls and with a mean age of 70.66.8 and 68.54.2 years, respectively. On the other hand, the values obtained in the present study are higher than those obtained by Bohannon16 for older adults between 80 and 89 years of age. However, in the present study, there was no difference in the AP trunk displacement during the FTSST among the groups. To our knowledge, no study has assessed trunk displacement during the FTSST in individuals with DM2 with or without DN. However, Trevisan et al11 showed AP displacement of the trunk in a population of women with osteoporosis during the FTSST, suggesting that a greater AP trunk displacement was related to compensation strategies during the test, relating to impaired motor skills that caused them to be more susceptible to falls.
The results show that the individuals with DM2 had an impairment of postural control compared with the individuals without DM2 in both the upright position and in dynamic situations, but individuals in the DN group had no more impairment of postural control in the variables studied than other subjects with DM2. A BBS score of 45 was considered the cutoff to determine risk of falling, and a TUG test time >10 seconds was used to determine mobility impairment; it is important to emphasize that the results obtained in the present study using these criteria do not reflect the higher percentage of falls actually reported by subjects in the group with DM2. Moreover, it was only possible to observe a higher risk of falls in the presence of neuropathy when percentage values were considered in the classification for the BBS, suggested by Berg et al,17 rather than by using the cutoff score. Proprioceptive pathways consist of large nerve fibers, and all patients included in the group with DN exhibited involvement of these fibers.4,37 However, the severity of proprioceptive impairment of the subjects in this group was not taken into account, a fact that may have contributed to the similarity in balance performance in the groups without and with neuropathy.
Study limitations The main limitation of this study was the variation in the severity of distal sensory large fiber polyneuropathy in the group of individuals with DN. Because there are few studies that evaluated the balance aspects in subjects with DM, it should be emphasized that our findings contribute to a better understanding of the changes in balance and functional mobility in individuals with DM2.
Conclusions Table 2 Maximum values for maximum AP displacement of the trunk during the FTSST and the time spent to perform the FTSST in all groups Groups
Rise (cm) Descent (cm) Time Spent (s)
DM2 without peripheral 13.64.1 14.83.4 neuropathy DM2 with peripheral 15.34.3 15.93.6 neuropathy Control 12.16.4 12.36.4 NOTE. Data are presented as mean SD. * P<.05 compared with controls.
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Individuals with DM2, compared with controls, have impaired postural control and functional strength. With regard to the variables studied, no difference was observed between individuals with DM2 and without distal neuropathy.
14.93.5* 15.12.7* 10.62.4
Suppliers a. MEB-9200J; Nihon Kohden, Tokyo, Japan. b. 3SPACE and Isotrak II; Polhemus, 40 Hercules Dr, Colchester, VT 05446. c. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
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Keywords Diabetic neuropathies; Rehabilitation
Corresponding author Prof. Dra. Daniela Cristina Carvalho de Abreu, PhD, Avenida Bandeirantes, 3900, Ribeira˜o Preto, SP, Brasil, CEP: 14049-900. E-mail address: [email protected].
Acknowledgments We thank the Bioengineering Unit (School of Medicine of University of Sa˜o Paulo-Ribeira˜o Preto) for the support provided.
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