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Relationship between skin resistance level and static balance in type II diabetic subjects
diabetes research and clinical practice 82 (2008) 335–339
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/diabres
Relationship between skin resistance level and static balance in type II diabetic subjects Eyyup Gulbandilar a,*, Ali Cimbiz b, Murat Sari c, Hilmi Ozden d a
Dumlupinar University, Faculty of Engineering, Department of Computer Engineering, 43100 Kutahya, Turkey Dumlupinar University, Health Institution of Higher Education, Department of Physical Therapy, 43100 Kutahya, Turkey c Pamukkale University, Faculty of Art and Science, Department of Mathematics, 20070 Denizli, Turkey d Eskisehir Osmangazi University, Faculty of Medicine, Department of Anatomy, 26000 Eskisehir, Turkey b
article info
abstract
Article history:
Diabetes mellitus is major cause leading to pathological changes in skin foot plantar area
Received 14 March 2008
(SFPA) and affected the static standing balance duration (SSBD). Skin resistance level (SRL) is
Received in revised form
related to skin conductance which changes in the presence of sweat. This study aims to find
28 July 2008
out the relationship between the SRL and SSBD in type II diabetic patients. Sixty-eight
Accepted 2 September 2008
voluntary students, 30 type II diabetic patients and 30 healthy non-diabetic subjects, were
Published on line 4 November 2008
participated to the study. The SSBD was measured on dominant and non-dominant legs. SRLs were recorded with two surface electrodes over the metatarsus heads and heel. The
Keywords:
SSBD of the healthy young group was found to be higher than the other groups (P < 0.001).
Direct current
The SRL values of the non-dominant leg in the diabetic group was found to be lower than the
Diabetes mellitus
others (P = 0.014). For dominant and non-dominant legs within each group, only the healthy
Static balance
young group has statistically difference (P = 0.012). A significant correlation was seen to be
Skin resistance
between the SRL and SSBD for only healthy non-diabetic group for the non-dominant leg. The relation between the SRL and SSBD is poor but very promising. Measurement of the SRL can be used in evaluating the inflammation of the diabetic foot. # 2008 Elsevier Ireland Ltd. All rights reserved.
1.
Introduction
The inhibitory component of the skin against given electrical current is called the electrical skin resistance [1]. Skin resistance level (SRL) is related to skin conductance which changes in the presence of sweat, a fluid composed of water and ions. It is determined by passing a weak current through the measuring changes in electricity flow or by measuring the current generated by the body itself. It has been correlated with emotion, attention and stress [2]. Skin foot plantar area (SFPA) has many mechanoreceptors (Pacinian, Meissner, Merkel and Ruffini) is sensitive to joint
pressure and tension. In addition: blood vessels, sweat gland activity and interstitial fluid exist under normal physiological conditions for SFPA. Loss of pressure sensitivity in SFPA, for instance in diabetic foot, etc., is related to risk of falling [3–5]. For evaluation of balance and risk of falling are used many dynamic and static balance tests. Static standing balance duration (SSBD) test is a commonly used for measurement of balance capabilities, and a significant predictor of falls [6]. Loss of sensation and autonomic problems can be seen in diabetic patients’ feet. In the corresponding patients; impairment of normal microcirculation and loss of sympathetic tonus give rise to arterio-venous shunts, edema and inflammation.
* Corresponding author. Tel.: +90 274 265 20 31x4454; fax: +90 274 265 20 66. E-mail addresses: [email protected] (E. Gulbandilar), [email protected] (A. Cimbiz), [email protected] (M. Sari), [email protected] (H. Ozden). 0168-8227/$ – see front matter # 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.diabres.2008.09.011
336
diabetes research and clinical practice 82 (2008) 335–339
Studies carried out on diabetic patients in the literature showed that the SFPA stiffened, impairment of the skin blood flow and sensation or absence in sweating affected the SSBD and played an important role for risk of falling [7–10]. There may be various approaches determining changes of the SFPA affecting the SSBD. Therefore, it was thought that measurement of the SRL is important to find out changes of the SFPA which cause crucial conclusions. Although there are many parameters affecting the SSBD, how changes of the SFPA in diabetic subjects affect the SSBD has not been investigated yet. Many researchers have focused on evaluation of the relation between the skin response and diabetic neuropathy [11–14]. To the best of authors’ knowledge, there has not been any research carried out on the relation between the SRL and SSBD in diabetic subjects. Therefore, the aim of the present study was to evaluate relationship between the SRL and SSBD in diabetic subjects.
2.
Fig. 1 – Simplified electrical model of the skin [2].
comfortably at the side. Subjects were tested on level tile flooring with athletic-type rubber-soled shoes. Subjects were allowed one practice trial for each of the balance tests. The test was accepted failure when the stance foot shifted in any way or the non-stance foot touched the ground. Each subject performed three trials and the best result of the three trials was recorded [3,15,16].
Materials and methods 2.2.
Sixty-eight healthy young voluntary students from the University of Dumlupinar, Physical Therapy and Rehabilitation School, in addition to 30 type II diabetic patients and 30 healthy non-diabetic subjects, in total 128 subjects, were participated to the study. All patients who had type II diabetes mellitus participated to the study from various clinics and hospitals in Ku¨tahya, Turkey, from February to September 2005. Criteria for having diabetes mellitus included the following: treatment with insulin or oral hypoglycemic agents, elevated fasting blood glucose 140 mg/dL. The exclusion criteria are: plantar ulcers at the moment of the evaluation, vision or hearing impairment, peripheral vascular disease, vestibulopathy history, or any neurological, muscular or rheumatic disease, history of abusive alcohol intake, partial or total amputation. The study had local research and ethics committee approval and all the subjects were given written consents. The hand used in writing and the leg used in kicking the ball are determined as the dominant side.
2.1.
Measurement of plantar foot skin resistance level
Any electrical model of the skin is seen in Fig. 1. In the figure, capacitor (C) represents the insulating layers of the stratum corneum, and the parallel resistor (R1) corresponds to the current path through the sweat gland ducts. R2 indicates the resistance of the deeper skin layers is relatively small [17]. In this study, direct current (5, 5 V) is applied to the skin. The direct current applied causes to increase in the resistance of the capacitor. The increasing of the resistance stops the current passing through the capacitor. Thus, the current applied passes through the resistances R1 and R2. Therefore this physical phenomenon gives the SRL of the part, of the skin tissue, to which the current was applied. The SRLs were recorded with two surface electrodes by the Digital Multimeter (DT-9923B) tool during standing on one leg (Fig. 2). Two carbon electrodes were placed over the 5 metatarsus heads and heel with conductive gel and applied to direct current between the two electrodes. After the measurements have reached a fixed value, the SRL values were recorded the final levels.
Static standing balance duration test measurement 2.3.
With the use of one leg standing position tests, SSBD was measured on dominant and non-dominant leg in two position; eyes open (60 s) and eyes closed (30 s) with arms held
Statistical analysis
SPSS 11.0 for Windows statistical program was used for all statistical analyses. Results were presented as mean S.D.
Fig. 2 – Skin resistance levels were recorded by the Digital Multimeter (DT-9923B) tool during standing on one leg.
337
diabetes research and clinical practice 82 (2008) 335–339
Table 1 – Demographic data of subjects.
Age (year) Height (cm) Body mass (kg) BMI (kg/m2) Diabetic duration (year) Insulin usage (year) Fasting blood glucose level (mg/dL) Gender (F/M)
Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
55.57 10.92 160.90 7.67 72.75 12.81 28.18 5.11 9.20 6.39 5.98 5.93 197.23 67.92 21/9
51.80 8.83 167.53 9.29 76.23 12.55 27.25 4.79 – – – 14/16
Healthy young group (n = 68) 20.24 1.35* 170.60 0.05 64.06 9.91* 21.96 2.84* – – – 36/32
BMI: body mass index. Data is presented as mean S.D. P < 0.05.
*
Statistical evaluation of the data was performed with one-way ANOVA (post hoc) test for comparison between the three groups (diabetic, non-diabetic and healthy young groups). Findings with an error probability value of less than 0.05 were considered as statistically significant.
the non-dominant leg. The dominant (r = 0.378, P = 0.039) and non-dominant (r = 0.368, P = 0.049) SSBD, when eyes closed, are correlated with the SRL value of the non-dominant leg in the healthy non-diabetic group.
4. 3.
Discussion
Results
The subjects’ demographic data are described in Table 1. No statistically significant differences between the diabetic and the healthy non-diabetic groups were found in demographic data. Age, body mass and body mass index values were observed statistically lower in the healthy young group than the others (P < 0.05) (Table 1). SSBDs were found to be statistically significant in all groups (P < 0.001) (Table 2). The SSBDs of diabetic and healthy non-diabetic groups were found to be lower than the SSBDs recorded for the healthy young group. In addition, the SSBD of the healthy non-diabetic group was seen to have higher durations than the SSBD of the diabetic group. The SRL values measured from the SFPA of the dominant leg were found to be statistically insignificant among the groups (P > 0.05). The SRL values from the SFPA of the nondominant leg in the diabetic group were found to be lower than the others (P = 0.014). When considering the dominant and non-dominant legs within each group, only the healthy young group has statistically difference (P = 0.012). Also the SRL values of the non-dominant side are seen to be higher than the dominant side, in the healthy young group (Table 3). Table 4 shows the correlation between the SRL and the SSBD. It has been found to be significant correlation between the SRL and the SSBD in only healthy non-diabetic group for
Many researchers have focused on evaluation of the relation between the skin response and diabetic neuropathy [11–14]. Specifically, Cimbiz et al. used healthy subjects to evaluate the relationship between the SRL and the SSBD [18]. In particular this study considered diabetic subjects to evaluate if there is a relation between the SRL and the SSBD. Human beings keep their balance when nerve signals from three different systems are accurately sent to and processed by the brain. The three systems are the vision, proprioception, and vestibular system. Humans seem to rely primarily on signals from the pressure sensors in the legs and proprioceptors to maintain good balance [8,9,15,19,20]. The SFPA is the first to touch the floor during standing and plays an extremely important role in supplying the nervous system with pressure and proprioception information [4,21]. Loss of pressure sensitivity, a measure of peripheral neuropathy, accounted for 3–6% of the relation between diabetes and risk of falling [3–5]. This kind of studies can be found in the literature. As known from the literature the process of impairment in the SSBD is speeding up for the diabetic subjects [3,6,22]. The diabetes mellitus has a clear effect on the SSBD in the same age group (50–60 years). The SRL values were found that there was a significant difference between the dominant and non-dominant legs in healthy young group. For the healthy young, use of the
Table 2 – Comparison of the static standing balance durations in groups. Static balance duration (s)
Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
Healthy young group (n = 68)
Dominant leg eyes open Dominant leg eyes close Non-dominant leg eyes open Non-dominant leg eyes close
26.77 18.66 a 8.00 6.13 a 19.50 16.24 a 4.63 3.80 a
45.53 18.81 b 17.47 10.80 b 41.37 20.45 b 16.50 10.43 b
56.32 9.35 c 21.99 9.62 c 56.93 9.33 c 20.75 10.04 c
Data is presented as Mean S.D. ANOVA (post hoc).
*
a,b,c
P < 0.001 (statistically significant within the groups).
Significance (P)* 0.000 0.000 0.000 0.000
338
diabetes research and clinical practice 82 (2008) 335–339
Table 3 – Comparison of foot plantar SRL of dominant and non-dominant leg in groups. Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
Healthy young group (n = 68)*
68.88 33.49 a 61.12 19.88 a
79.85 32.09 a 78.80 28.81 b
66.87 20.81 a 74.14 28.25 b
Dominant leg SRL (kV) Non-dominant leg SRL (kV)
Significance (P)** 0.090 0.014
Data is presented as mean S.D., SRL: skin resistance level. a,bP < 0.05 (statistically significant within the groups). Non-dominant leg SRL statistically higher than dominant leg in healthy young group (P < 0.012). ** ANOVA (post hoc). *
dominant side causes to sweating, increasing in ion concentration and being lower SRL values comparison to the nondominant side. It was seen that the difference of the SRL values between the dominant and non-dominant sides are getting smaller in the healthy non-diabetic group at further ages. It was thought that aging might cause to decreasing in interstitial fluid, ion concentration and capillarization of the SFPA and stiffness of it, and therefore these changes may lead to increasing in the SRL values at further ages. It was seen that the SRL values of the diabetic group are close to the SRL values of the healthy young group. This observation reminds us a response of inflammation more than a healthy SFPA. In the meantime, Lindholm-Sethson et al. pointed out the possibility that the lesions of neuropathy and microangiopathy were associated with the differences in skin resistance findings [13]. Nabuurs-Franssen et al. studied that type II diabetes polyneuropathy is associated with multiple abnormalities in the microcirculation of the foot, characterized by reduced capillary blood flow, an enhanced reduction in skin blood flux and impaired fluid filtration after sitting up [14]. To determine nerve fiber number and nerve lengths, Hirai et al. performed a quantitative analysis was on nerve fibers of the epidermis and the dermis and on nerves surrounding sweat glands. They found out that the number of epidermal nerves fiber number and nerve lengths around sweat glands were significantly decreased in diabetic patients compared with control subjects [23]. Despite much increasing in the volume of studies carried
out on the SRL of the diabetic subjects in the literature, the corresponding studies are not as promising as desired. Due to impairing in skin microcirculation and foot swelling rate, decreasing in nerves fiber number and nerve lengths, stiffened SFPA are expected to cause decreasing in ion concentration, and therefore increasing in the SRL of diabetic foot. However, in the current study, the SRL of the diabetic subjects was found to be lower than the SRL of the non-diabetic and healthy young subjects. The SRL values of the diabetic subjects show that response of inflammation is of more priority opposite to pathological changes in the SFPA pointed out by the above researchers. This result is supported by the works of Flynn and Tooke and Leslie et al. In their works, another component of the inflammation is the skin temperature measured high in the feet of diabetic subjects. When inflammation process takes place, the skin temperature and the amount of interstitial fluid increase [24–26]. Therefore decreasing in the SRL values is as usual. It was also found to be an inverse relation between the SSBD and the SRL in healthy groups, even though it is not statistically significant. For the diabetic subjects, the more increasing in the SRL the more increasing in the SSBD and vice versa. This is again not statistically significant. It was thought that this result again stems from inflammation of SFPA. Main limitation of the present study is the absence of a diabetic with neuropathy group. Therefore a further study can be organized with the presence of a diabetic with neuropathy
Table 4 – Correlation between static standing balance duration and SRL of foot. Static balance duration
Diabetic group Dominant SRL
Non-dominant SRL
Healthy non-diabetic group Dominant SRL
Non-dominant SRL
Healthy young group Dominant SRL
Non-dominant SRL
Dominant leg eyes open r P
0.123 0.516
0.233 0.216
0.184 0.329
0.117 0.536
0.074 0.550
0.045 0.716
Dominant leg eyes close r P
0.180 0.342
0.204 0.279
0.054 0.777
0.378* 0.039
0.008 0.946
0.075 0.544
Non-dominant leg eyes open r P
0.068 0.720
0.193 0.306
0.136 0.472
0.139 0.462
0.151 0.218
0.104 0.398
Non-dominant leg eyes close r P
0.099 0.603
0.105 0.582
0.072 0.705
0.368* 0.049
0.079 0.523
0.035 0.775
Data shows correlation coefficient and P-value. SRL: skin resistance level. Correlation is significant at the 0.05 level.
*
diabetes research and clinical practice 82 (2008) 335–339
group under the conditions of inflammational changes such as pain, sweating, increasing of temperature, edema, etc. The relation between the SRL values and the SSBD can also be investigated with the use of other balance tests. For further research, also attention can be concentrated on comparison of the SRL and histochemical works. As conclusions: (i) changes of SFPA can be evaluated by the SRL values; (ii) measurement of the SRL is user-friendly and cost effective in evaluating the inflammation of the diabetic foot; (iii) although there is a poor relation between the SRL and the SSBD, the present results are believed to be very promising.
Conflict of interest There are no conflicts of interest.
references
[1] S.H. Cho, S.I. Chun, The basal electrical skin resistance of acupuncture points in normal subjects, Yonsei Med. J. 35 (1994) 464–474. [2] R.B. Clariana, Media research with a galvanic skin response biosensor: some kids work up a sweat. (1992). Available from URL: http://www.personal.psu.edu/faculty/r/b/rbc4/ media_research_with_GSR.htm. [3] A. Cimbiz, O. Cakir, Evaluation of balance and physical fitness in diabetic neuropathic patients, J. Diab. Complications 19 (3) (2005) 160–164. [4] E.M. Gutierrez, M.D. Heber, D. Dealva, J.A. Ashton-Miller, Mild diabetic neuropathy affects ankle motor function, Clin. Biomech. (Bristol, Avon) 16 (2001) 522–528. [5] J.K. Richardson, Factors associated with falls in older patients with diffuse polyneuropathy, J. Am. Geriatr. Soc. 50 (2002.) (1767-73). [6] E.A. Hurvitz, J.K. Richardson, R.A. Werner, A.M. Ruhl, M.R. Dixon, Unipedal stance testing as an indicator of fall risk among older outpatients, Arch. Phys. Med. Rehabil. 81 (2000) 587–591. [7] A. Gefen, Plantar soft tissue loading under the medial metatarsals in the standing diabetic foot, Med. Eng. Phys. 25 (2003) 491–499. [8] A.I. Vinik, T. Erbas, K.B. Stansberry, G.L. Pittenger, Small fiber neuropathy and neurovascular disturbances in diabetes mellitus, Exp. Clin. Endocrinol. Diab. 109 (2001) 451–473. [9] H.E. Resnick, K.B. Stansberry, T.B. Harris, M. Tirivedi, K. Smith, P. Morgan, et al., Diabetes, peripheral neuropathy, and old age disability, Muscle Nerve 25 (2002) 43–50. [10] A.J. Boulton, C.A. Hardisty, R.P. Betts, C.I. Franks, R.C. Worth, J.D. Ward, et al., Dynamic foot pressure and other studies as diagnostic and management aids in diabetic neuropathy, Diab. Care 6 (1) (1983) 26–33.
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[11] A.F. Macleod, S.A. Smith, T. Cowell, P.R. Richardson, P.H. Sonksen, Non-cardiac autonomic tests in diabetes: use of the galvanic skin response, Diab. Med. 8 (1991) 67–70. [12] K. Takebayashi, Y. Aso, R. Sugita, Y. Takemura, T. Inukai, Relationship between sympathetic skin response and power spectral analysis of heart rate variation in patients with type 2 diabetes, J. Diab. Complications 18 (2004) 224–228. [13] B. Lindholm-Sethson, S. Han, S. Ollmar, I. Nicander, G. Jonsson, F. Lithner, et al., Multivariate analysis of skin impedance data in long-term type 1 diabetic patients, Chemometr. Intel. Lab. Syst. 44 (1998) 381–394. [14] M.H. Nabuurs-Franssen, A.J.H.M. Houben, J.E. Tooke, N.C. Schaper, The effect of polyneuropathy on foot microcirculation in type II diabetes, Diabetologia 45 (2002) 1164–1171. [15] S. Huroyuki, Y. Uchiyama, S. Kakurai, Specific effects of balance and gait exercises on physical function among the frail elderly, Clin. Rehabil. 17 (2003) 472–479. [16] M. Ozdirenc, S. Biberoglu, A. Ozcan, Evaluation of physical fitness in patients with type 2 diabetes mellitus, Diab. Res. Clin. Pract. 60 (2003) 171–176. [17] F. Schaefer, W. Boucsein, Comparison of electrodermal constant voltage and constant current recording techniques using the phase angle between alternating voltage and current, Psychophysiology 37 (2000) 85–91. [18] A. Cimbiz, E. Gulbandilar, V. Bayazıt, Y. Ozay, H. Dayioglu, Relation between skin resistance levels and one leg standing balance in healthy subjects, J. Med. Sci. 6 (2) (2006) 286–291. [19] A.J. Vander, J.H. Sherman, D.S. Luciano, Human Physiology: The Mechanism of Body Function, 6th ed., McGraw-Hill, New York, 1994, pp. 233–271. [20] J.N. Bernier, D.H. Perrin, Effect of coordination training on proprioception of the functionally unstable ankle, J. Orthop. Sports Phys. Ther. 27 (1998) 264–275. [21] H. Andersen, Muscular endurance in long-term IDDM patients, Diab. Care 21 (1998) 604–649. [22] A. Goldberg, J.W. Russell, N.B. Alexander, Standing balance and trunk position sense in impaired glucose tolerance (IGT)-related peripheral neuropathy, J. Neurol. Sci. 270 (2008) 165–171. [23] A. Hirai, H. Yasuda, M. Joko, T. Maeda, R. Kikkawa, Evaluation of diabetic neuropathy through the quantitation of cutaneous nerves, J. Neurol. Sci. 172 (1) (2000) 55–62. [24] M.D. Flynn, J.E. Tooke, Diabetic neuropathy and the microcirculation, Diab. Med. 12 (1995) 298–301. [25] P. Leslie, R.T. Jung, T.E. Isles, J. Baty, R.W. Newton, P. Illingworth, Effect of optimum glycemic control with continuos subcutaneous insulin infusion on energy expenditure in type 1 diabetes mellitus, Br. Med. J. 293 (1986) 1121–1126. [26] E.J. Boyko, J.H. Ahroni, V.L. Stensel, Skin temperature in the neuropathic diabetic foot, J. Diab. Complications 15 (2001) 260–264.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/diabres
Relationship between skin resistance level and static balance in type II diabetic subjects Eyyup Gulbandilar a,*, Ali Cimbiz b, Murat Sari c, Hilmi Ozden d a
Dumlupinar University, Faculty of Engineering, Department of Computer Engineering, 43100 Kutahya, Turkey Dumlupinar University, Health Institution of Higher Education, Department of Physical Therapy, 43100 Kutahya, Turkey c Pamukkale University, Faculty of Art and Science, Department of Mathematics, 20070 Denizli, Turkey d Eskisehir Osmangazi University, Faculty of Medicine, Department of Anatomy, 26000 Eskisehir, Turkey b
article info
abstract
Article history:
Diabetes mellitus is major cause leading to pathological changes in skin foot plantar area
Received 14 March 2008
(SFPA) and affected the static standing balance duration (SSBD). Skin resistance level (SRL) is
Received in revised form
related to skin conductance which changes in the presence of sweat. This study aims to find
28 July 2008
out the relationship between the SRL and SSBD in type II diabetic patients. Sixty-eight
Accepted 2 September 2008
voluntary students, 30 type II diabetic patients and 30 healthy non-diabetic subjects, were
Published on line 4 November 2008
participated to the study. The SSBD was measured on dominant and non-dominant legs. SRLs were recorded with two surface electrodes over the metatarsus heads and heel. The
Keywords:
SSBD of the healthy young group was found to be higher than the other groups (P < 0.001).
Direct current
The SRL values of the non-dominant leg in the diabetic group was found to be lower than the
Diabetes mellitus
others (P = 0.014). For dominant and non-dominant legs within each group, only the healthy
Static balance
young group has statistically difference (P = 0.012). A significant correlation was seen to be
Skin resistance
between the SRL and SSBD for only healthy non-diabetic group for the non-dominant leg. The relation between the SRL and SSBD is poor but very promising. Measurement of the SRL can be used in evaluating the inflammation of the diabetic foot. # 2008 Elsevier Ireland Ltd. All rights reserved.
1.
Introduction
The inhibitory component of the skin against given electrical current is called the electrical skin resistance [1]. Skin resistance level (SRL) is related to skin conductance which changes in the presence of sweat, a fluid composed of water and ions. It is determined by passing a weak current through the measuring changes in electricity flow or by measuring the current generated by the body itself. It has been correlated with emotion, attention and stress [2]. Skin foot plantar area (SFPA) has many mechanoreceptors (Pacinian, Meissner, Merkel and Ruffini) is sensitive to joint
pressure and tension. In addition: blood vessels, sweat gland activity and interstitial fluid exist under normal physiological conditions for SFPA. Loss of pressure sensitivity in SFPA, for instance in diabetic foot, etc., is related to risk of falling [3–5]. For evaluation of balance and risk of falling are used many dynamic and static balance tests. Static standing balance duration (SSBD) test is a commonly used for measurement of balance capabilities, and a significant predictor of falls [6]. Loss of sensation and autonomic problems can be seen in diabetic patients’ feet. In the corresponding patients; impairment of normal microcirculation and loss of sympathetic tonus give rise to arterio-venous shunts, edema and inflammation.
* Corresponding author. Tel.: +90 274 265 20 31x4454; fax: +90 274 265 20 66. E-mail addresses: [email protected] (E. Gulbandilar), [email protected] (A. Cimbiz), [email protected] (M. Sari), [email protected] (H. Ozden). 0168-8227/$ – see front matter # 2008 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.diabres.2008.09.011
336
diabetes research and clinical practice 82 (2008) 335–339
Studies carried out on diabetic patients in the literature showed that the SFPA stiffened, impairment of the skin blood flow and sensation or absence in sweating affected the SSBD and played an important role for risk of falling [7–10]. There may be various approaches determining changes of the SFPA affecting the SSBD. Therefore, it was thought that measurement of the SRL is important to find out changes of the SFPA which cause crucial conclusions. Although there are many parameters affecting the SSBD, how changes of the SFPA in diabetic subjects affect the SSBD has not been investigated yet. Many researchers have focused on evaluation of the relation between the skin response and diabetic neuropathy [11–14]. To the best of authors’ knowledge, there has not been any research carried out on the relation between the SRL and SSBD in diabetic subjects. Therefore, the aim of the present study was to evaluate relationship between the SRL and SSBD in diabetic subjects.
2.
Fig. 1 – Simplified electrical model of the skin [2].
comfortably at the side. Subjects were tested on level tile flooring with athletic-type rubber-soled shoes. Subjects were allowed one practice trial for each of the balance tests. The test was accepted failure when the stance foot shifted in any way or the non-stance foot touched the ground. Each subject performed three trials and the best result of the three trials was recorded [3,15,16].
Materials and methods 2.2.
Sixty-eight healthy young voluntary students from the University of Dumlupinar, Physical Therapy and Rehabilitation School, in addition to 30 type II diabetic patients and 30 healthy non-diabetic subjects, in total 128 subjects, were participated to the study. All patients who had type II diabetes mellitus participated to the study from various clinics and hospitals in Ku¨tahya, Turkey, from February to September 2005. Criteria for having diabetes mellitus included the following: treatment with insulin or oral hypoglycemic agents, elevated fasting blood glucose 140 mg/dL. The exclusion criteria are: plantar ulcers at the moment of the evaluation, vision or hearing impairment, peripheral vascular disease, vestibulopathy history, or any neurological, muscular or rheumatic disease, history of abusive alcohol intake, partial or total amputation. The study had local research and ethics committee approval and all the subjects were given written consents. The hand used in writing and the leg used in kicking the ball are determined as the dominant side.
2.1.
Measurement of plantar foot skin resistance level
Any electrical model of the skin is seen in Fig. 1. In the figure, capacitor (C) represents the insulating layers of the stratum corneum, and the parallel resistor (R1) corresponds to the current path through the sweat gland ducts. R2 indicates the resistance of the deeper skin layers is relatively small [17]. In this study, direct current (5, 5 V) is applied to the skin. The direct current applied causes to increase in the resistance of the capacitor. The increasing of the resistance stops the current passing through the capacitor. Thus, the current applied passes through the resistances R1 and R2. Therefore this physical phenomenon gives the SRL of the part, of the skin tissue, to which the current was applied. The SRLs were recorded with two surface electrodes by the Digital Multimeter (DT-9923B) tool during standing on one leg (Fig. 2). Two carbon electrodes were placed over the 5 metatarsus heads and heel with conductive gel and applied to direct current between the two electrodes. After the measurements have reached a fixed value, the SRL values were recorded the final levels.
Static standing balance duration test measurement 2.3.
With the use of one leg standing position tests, SSBD was measured on dominant and non-dominant leg in two position; eyes open (60 s) and eyes closed (30 s) with arms held
Statistical analysis
SPSS 11.0 for Windows statistical program was used for all statistical analyses. Results were presented as mean S.D.
Fig. 2 – Skin resistance levels were recorded by the Digital Multimeter (DT-9923B) tool during standing on one leg.
337
diabetes research and clinical practice 82 (2008) 335–339
Table 1 – Demographic data of subjects.
Age (year) Height (cm) Body mass (kg) BMI (kg/m2) Diabetic duration (year) Insulin usage (year) Fasting blood glucose level (mg/dL) Gender (F/M)
Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
55.57 10.92 160.90 7.67 72.75 12.81 28.18 5.11 9.20 6.39 5.98 5.93 197.23 67.92 21/9
51.80 8.83 167.53 9.29 76.23 12.55 27.25 4.79 – – – 14/16
Healthy young group (n = 68) 20.24 1.35* 170.60 0.05 64.06 9.91* 21.96 2.84* – – – 36/32
BMI: body mass index. Data is presented as mean S.D. P < 0.05.
*
Statistical evaluation of the data was performed with one-way ANOVA (post hoc) test for comparison between the three groups (diabetic, non-diabetic and healthy young groups). Findings with an error probability value of less than 0.05 were considered as statistically significant.
the non-dominant leg. The dominant (r = 0.378, P = 0.039) and non-dominant (r = 0.368, P = 0.049) SSBD, when eyes closed, are correlated with the SRL value of the non-dominant leg in the healthy non-diabetic group.
4. 3.
Discussion
Results
The subjects’ demographic data are described in Table 1. No statistically significant differences between the diabetic and the healthy non-diabetic groups were found in demographic data. Age, body mass and body mass index values were observed statistically lower in the healthy young group than the others (P < 0.05) (Table 1). SSBDs were found to be statistically significant in all groups (P < 0.001) (Table 2). The SSBDs of diabetic and healthy non-diabetic groups were found to be lower than the SSBDs recorded for the healthy young group. In addition, the SSBD of the healthy non-diabetic group was seen to have higher durations than the SSBD of the diabetic group. The SRL values measured from the SFPA of the dominant leg were found to be statistically insignificant among the groups (P > 0.05). The SRL values from the SFPA of the nondominant leg in the diabetic group were found to be lower than the others (P = 0.014). When considering the dominant and non-dominant legs within each group, only the healthy young group has statistically difference (P = 0.012). Also the SRL values of the non-dominant side are seen to be higher than the dominant side, in the healthy young group (Table 3). Table 4 shows the correlation between the SRL and the SSBD. It has been found to be significant correlation between the SRL and the SSBD in only healthy non-diabetic group for
Many researchers have focused on evaluation of the relation between the skin response and diabetic neuropathy [11–14]. Specifically, Cimbiz et al. used healthy subjects to evaluate the relationship between the SRL and the SSBD [18]. In particular this study considered diabetic subjects to evaluate if there is a relation between the SRL and the SSBD. Human beings keep their balance when nerve signals from three different systems are accurately sent to and processed by the brain. The three systems are the vision, proprioception, and vestibular system. Humans seem to rely primarily on signals from the pressure sensors in the legs and proprioceptors to maintain good balance [8,9,15,19,20]. The SFPA is the first to touch the floor during standing and plays an extremely important role in supplying the nervous system with pressure and proprioception information [4,21]. Loss of pressure sensitivity, a measure of peripheral neuropathy, accounted for 3–6% of the relation between diabetes and risk of falling [3–5]. This kind of studies can be found in the literature. As known from the literature the process of impairment in the SSBD is speeding up for the diabetic subjects [3,6,22]. The diabetes mellitus has a clear effect on the SSBD in the same age group (50–60 years). The SRL values were found that there was a significant difference between the dominant and non-dominant legs in healthy young group. For the healthy young, use of the
Table 2 – Comparison of the static standing balance durations in groups. Static balance duration (s)
Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
Healthy young group (n = 68)
Dominant leg eyes open Dominant leg eyes close Non-dominant leg eyes open Non-dominant leg eyes close
26.77 18.66 a 8.00 6.13 a 19.50 16.24 a 4.63 3.80 a
45.53 18.81 b 17.47 10.80 b 41.37 20.45 b 16.50 10.43 b
56.32 9.35 c 21.99 9.62 c 56.93 9.33 c 20.75 10.04 c
Data is presented as Mean S.D. ANOVA (post hoc).
*
a,b,c
P < 0.001 (statistically significant within the groups).
Significance (P)* 0.000 0.000 0.000 0.000
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diabetes research and clinical practice 82 (2008) 335–339
Table 3 – Comparison of foot plantar SRL of dominant and non-dominant leg in groups. Diabetic group (n = 30)
Healthy non-diabetic group (n = 30)
Healthy young group (n = 68)*
68.88 33.49 a 61.12 19.88 a
79.85 32.09 a 78.80 28.81 b
66.87 20.81 a 74.14 28.25 b
Dominant leg SRL (kV) Non-dominant leg SRL (kV)
Significance (P)** 0.090 0.014
Data is presented as mean S.D., SRL: skin resistance level. a,bP < 0.05 (statistically significant within the groups). Non-dominant leg SRL statistically higher than dominant leg in healthy young group (P < 0.012). ** ANOVA (post hoc). *
dominant side causes to sweating, increasing in ion concentration and being lower SRL values comparison to the nondominant side. It was seen that the difference of the SRL values between the dominant and non-dominant sides are getting smaller in the healthy non-diabetic group at further ages. It was thought that aging might cause to decreasing in interstitial fluid, ion concentration and capillarization of the SFPA and stiffness of it, and therefore these changes may lead to increasing in the SRL values at further ages. It was seen that the SRL values of the diabetic group are close to the SRL values of the healthy young group. This observation reminds us a response of inflammation more than a healthy SFPA. In the meantime, Lindholm-Sethson et al. pointed out the possibility that the lesions of neuropathy and microangiopathy were associated with the differences in skin resistance findings [13]. Nabuurs-Franssen et al. studied that type II diabetes polyneuropathy is associated with multiple abnormalities in the microcirculation of the foot, characterized by reduced capillary blood flow, an enhanced reduction in skin blood flux and impaired fluid filtration after sitting up [14]. To determine nerve fiber number and nerve lengths, Hirai et al. performed a quantitative analysis was on nerve fibers of the epidermis and the dermis and on nerves surrounding sweat glands. They found out that the number of epidermal nerves fiber number and nerve lengths around sweat glands were significantly decreased in diabetic patients compared with control subjects [23]. Despite much increasing in the volume of studies carried
out on the SRL of the diabetic subjects in the literature, the corresponding studies are not as promising as desired. Due to impairing in skin microcirculation and foot swelling rate, decreasing in nerves fiber number and nerve lengths, stiffened SFPA are expected to cause decreasing in ion concentration, and therefore increasing in the SRL of diabetic foot. However, in the current study, the SRL of the diabetic subjects was found to be lower than the SRL of the non-diabetic and healthy young subjects. The SRL values of the diabetic subjects show that response of inflammation is of more priority opposite to pathological changes in the SFPA pointed out by the above researchers. This result is supported by the works of Flynn and Tooke and Leslie et al. In their works, another component of the inflammation is the skin temperature measured high in the feet of diabetic subjects. When inflammation process takes place, the skin temperature and the amount of interstitial fluid increase [24–26]. Therefore decreasing in the SRL values is as usual. It was also found to be an inverse relation between the SSBD and the SRL in healthy groups, even though it is not statistically significant. For the diabetic subjects, the more increasing in the SRL the more increasing in the SSBD and vice versa. This is again not statistically significant. It was thought that this result again stems from inflammation of SFPA. Main limitation of the present study is the absence of a diabetic with neuropathy group. Therefore a further study can be organized with the presence of a diabetic with neuropathy
Table 4 – Correlation between static standing balance duration and SRL of foot. Static balance duration
Diabetic group Dominant SRL
Non-dominant SRL
Healthy non-diabetic group Dominant SRL
Non-dominant SRL
Healthy young group Dominant SRL
Non-dominant SRL
Dominant leg eyes open r P
0.123 0.516
0.233 0.216
0.184 0.329
0.117 0.536
0.074 0.550
0.045 0.716
Dominant leg eyes close r P
0.180 0.342
0.204 0.279
0.054 0.777
0.378* 0.039
0.008 0.946
0.075 0.544
Non-dominant leg eyes open r P
0.068 0.720
0.193 0.306
0.136 0.472
0.139 0.462
0.151 0.218
0.104 0.398
Non-dominant leg eyes close r P
0.099 0.603
0.105 0.582
0.072 0.705
0.368* 0.049
0.079 0.523
0.035 0.775
Data shows correlation coefficient and P-value. SRL: skin resistance level. Correlation is significant at the 0.05 level.
*
diabetes research and clinical practice 82 (2008) 335–339
group under the conditions of inflammational changes such as pain, sweating, increasing of temperature, edema, etc. The relation between the SRL values and the SSBD can also be investigated with the use of other balance tests. For further research, also attention can be concentrated on comparison of the SRL and histochemical works. As conclusions: (i) changes of SFPA can be evaluated by the SRL values; (ii) measurement of the SRL is user-friendly and cost effective in evaluating the inflammation of the diabetic foot; (iii) although there is a poor relation between the SRL and the SSBD, the present results are believed to be very promising.
Conflict of interest There are no conflicts of interest.
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