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| ORIGINAL ARTICLE |
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| Year : 2016 | Volume
: 53
| Issue : 2 | Page : 124-129 |
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Transcutaneous nerve stimulation versus aerobic exercise in diabetic neuropathy
Zahra M. H. Serry1, Gehan Mossa1, Hala Elhabashy2, Soad Elsayed3, Reem Elhadidy2, Radwa M Azmy2, Ahmed Mokhtar1
1 Department of Physical Therapy, Cairo University, Cairo, Egypt
2 Department of Clinical Neurophysiology, Cairo University, Cairo, Egypt
3 Department of Internal Medicine, Cairo University, Cairo, Egypt
| Date of Submission | 08-Sep-2014 |
| Date of Acceptance | 15-Nov-2014 |
| Date of Web Publication | 2-Jun-2016 |
Correspondence Address:
Hala Elhabashy
MD, Department of Clinical Neurophysiology, Cairo University, Cairo
Egypt
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/1110-1083.183449
Background
Diabetic peripheral neuropathy (DPN) is the most common complication of diabetes, which is frequently associated with pain. Studies targeting the painful DPN are necessary to support clinical decision-making.
Objective
The aim of the present study was to investigate the efficacy of transcutaneous electric nerve stimulation (TENS) versus aerobic exercise, and to compare them with regular pharmacological therapy in patients with DPN, using sensory nerve conduction study and the visual analogue scale (VAS).
Patients and methods
This study included 60 diabetic patients with a history of DPN for 5 years. Patients were divided into three equal groups, all receiving regular pharmacological therapy. Group A received TENS of both lower limbs, three times per week. Group B received aerobic exercise. Group C received only pharmacological therapy. Patients were assessed before and 8 weeks after treatment. The VAS was used to measure the pain intensity before and after treatment, and the medial plantar nerve conduction velocity (NCV) to assess nerve function.
Results
Group A and B only showed a significant statistical difference between pretreatment and post-treatment pain intensity on VAS, with 41.67 and 16.67% improvement on the VAS, respectively. There was no statistically significant difference in pretreatment and post-treatment as regards the medial plantar NCV in any of the groups.
Conclusion
TENS, of moderate intensity, carried out at 14 Hz, with a pulse width of 250 ms, for 30 min and three times a week is more efficient than aerobic exercise training program in relieving pain in patients with DPN, whereas neither TENS nor exercise showed any significant effect on medial plantar conduction velocity (CV) in patients with DPN. Keywords: Conduction velocity, diabetic peripheral neuropathy, medial plantar nerve, transcutaneous electric nerve stimulation, visual analogue scale
How to cite this article:
Serry ZM, Mossa G, Elhabashy H, Elsayed S, Elhadidy R, Azmy RM, Mokhtar A. Transcutaneous nerve stimulation versus aerobic exercise in diabetic neuropathy. Egypt J Neurol Psychiatry Neurosurg 2016;53:124-9 |
How to cite this URL:
Serry ZM, Mossa G, Elhabashy H, Elsayed S, Elhadidy R, Azmy RM, Mokhtar A. Transcutaneous nerve stimulation versus aerobic exercise in diabetic neuropathy. Egypt J Neurol Psychiatry Neurosurg [serial online] 2016 [cited 2023 Jun 6];53:124-9. Available from: http://www.ejnpn.eg.net/text.asp?2016/53/2/124/183449 |
| Introduction | |  |
Diabetic peripheral neuropathy (DPN) is a common complication estimated to affect 30-50% of diabetic patients [1]. DPN affects sensory, autonomic, and motor neurons, and nearly every type of nerve fiber is vulnerable [2]. Diabetes and prediabetes, including both impaired glucose tolerance and impaired fasting glucose, are frequently associated with pure small fiber neuropathy; yet, large fiber involvement is seen more often [3]. Diabetics may also experience an acute painful small fiber neuropathy associated with rapid glycemic control, referred to as insulin neuritis or treatment-induced neuropathy [4].
Most small fiber neuropathies occur in a length-dependent fashion, resulting in sensory dysfunction in a stocking distribution in the lower extremities. A glove-like loss affects the upper extremities in more advanced cases. Rarely, a non-length-dependent neuropathy, involving the trunk, face, proximal limbs, or other focal areas, occur [5],[6].
Around 16% of the diabetic patients suffer from a painful form of neuropathy that can be difficult to treat [7]. Many pharmacologic and nonpharmacologic options, published in an evidence-based guideline by the American Academy of Neurology (AAN) [8], help guide physicians regarding the strength of evidence for these various therapies. The first step in the management of DPN is to control the blood glucose level. Management of painful neuropathy can be challenging as patients may not get good response to the pharmacological options and the medications used are associated with side effects, which the patients may find difficult to tolerate [9]. The current evidence supports nonpharmacological treatment as transcutaneous electric nerve stimulation (TENS), acupuncture and psychological support [10],[11]. According to the AAN [8] guideline, TENS should be considered as a level B recommendation for pain treatment. TENS is the application of a mild electrical current to the cutaneous nerve using surface electrodes. It is used extensively for pain relief in various disorders [12]. The mechanism is related to both neuronal modulation and increase in the endogenous opioid-like substance (dynorphins, endorphins, enkephalins) within the central nervous system (CNS) [13], with a significant increase in pain threshold after TENS application [14].
Exercise can also improve mental health and mood. Regular aerobic exercise reduces the amount of adrenal hormones and increases the amount of endorphins, which is a powerful pain-relieving and mood-elevating chemical in the brain [15]. In addition, it improves the blood circulation, which strengthens nerve tissues by increasing the flow of oxygen [16].
Nerve conduction studies (NCSs) are the most objective noninvasive measures of nerve function, which represent a valuable tool of evaluation of neuropathy. However, in all small-fiber polyneuropathies, the main drawback of NCS is that small myelinated and unmyelinated nerve fibers, which are affected early in the disease course of diabetic neuropathy, do not contribute to the sensory action potential detected by routine NCS. The sensory action potential is altered only after involvement of larger myelinated fibers, which is often a late event in patients with diabetes. Electrophysiological data must, therefore, always be evaluated in a clinical context [17].
| Aim | | |
The aim of the present study was to investigate the efficacy of TENS versus aerobic exercise, and to compare them with regular pharmacological therapy alone in patients with DPN, using sensory NCS and visual analogue scale (VAS).
| Patients and methods | | |
A total of 60 patients (32 women and 28 men), aged 45-60 years, with type II diabetes mellitus (for ≥10 years) and DPN for at least 5 years were selected from the Outpatient Clinics of El Agouza and Kasr Al-Aini Hospitals. Patients were randomly divided into three equal groups.
Group A (TENS group) comprised 20 patients (12 women and eight men), who received TENS on both lower limbs, three times per week for 8 weeks, in addition to their regular pharmacological therapy.
Group B (exercise group) comprised 20 patients (10 women and 10 men), who received aerobic exercise on a stationary bicycle, three times per week for 8 weeks, in addition to their regular pharmacological therapy.
Group C (pharmacological group) comprised 20 patients (10 women and 10 men), who received only their regular pharmacological therapy for peripheral neuropathy (nerve growth stimulant; vitamin B complex) and oral hypoglycemic drugs or insulin.
Patients included in this study were ambulant and independent. Their blood glucose level HbA1c was less than 6.5%. The strength of the muscles in the lower limbs was not less than grade 4 according to manual muscle testing. The BMI ranged from 18.5 to 29.9 kg/m 2 .
We excluded patients who had life-threatening diseases like renal failure, myocardial infarction, and heart failure; those who had sensory manifestations due to any other diseases (lumbar disc prolapsed); those with circulatory problems such as intermittent claudications, skin diseases, or foot ulcers; and patients with BMI greater than or equal to 30 kg/m 2 .
Methods
(1) VAS: this scale was used to measure the pain intensity before and after treatment. The scale used for this test was 10 cm in length with two labeled endpoints (0 = no pain and 10 = most pain ever). The patients were asked to determine the intensity of pain on the length of the pain scale according to its severity (from 0 to 10).
(2) Sensory NCS was carried out using (two channels) Dantec Keypoint 9033 (Dantec Keypoint 9033, USA) to study the medial plantar sensory nerve conduction velocity (SCV) before and after treatment. Stimulus duration was 0.2 ms at a rate of 1 Hz, 10-20 mV/division, with a filter setting of 2 kHz-20 Hz. The recording electrode was placed over the first metatarsophalangeal joint and the reference electrode over the tip of the big toe, whereas the ground was placed over the dorsum of the foot. We stimulated the nerve below and behind the medial malleolus. NCV of the medial nerve was considered normal for values greater than or equal to 35 m/s [18].
TENS was carried out for patients in group A, on both lower limbs, by using a portable TENS unit (two channel TENS 210; Mettler, USA). It was used with four adhesive electrodes placed on the lower limbs as follows: one electrode at the lower border of medial tibial condyle, and another electrode placed 3 inches above medial malleolus, close to the tibia of the right lower limb (first channel); similarly, the remaining two electrodes were placed over the left leg. The patients lay in comfortable supine position and the device intensity was adjusted till strong rhythmic visible muscle contractions were seen, with a low frequency of 15 Hz and a pulse width of 250 μs. Session duration was 30 min, three times per week for 8 weeks, according to the protocol used in a study by Hamza et al. [19].
All patients in group B were subjected to the exercise training program for a 50 minute session, 3 times per week for 8 weeks. Each training session consisted of three phases [20]: (i) the warm up phase, which comprised 5 min of stretching of calf, hamstring, and adductor muscles to warm up the skeletal muscles, heart, and lungs for a progressive increase in the exercise intensity; (ii) the active phase, which comprised 40 min of aerobic exercises of moderate intensity on a stationary bicycle, with a training heart rate of 50-70% of the maximal heart rate; and (iii) the cool down phase, which comprised 5 min of light aerobic and stretching exercises.
This research was approved by the local ethical committee. All patients were informed about the nature of the study, and signed an informed consent. All patients were evaluated before and after the study for pain intensity and nerve conduction velocity.
Statistical analysis
Descriptive statistics in the form of mean and SD were used for all variables. The Mann-Whitney U-test was used to compare pretreatment and post-treatment results within each group for pain intensity, whereas the Kruskal-Wallis test was used to compare pretreatment and post-treatment results among the three groups for pain intensity. Paired t-test was used to compare pretreatment and post-treatment results within each group for nerve conduction velocity, whereas analysis of variance was used to compare pretreatment and post-treatment results among the three groups for nerve conduction velocity. A P value of less than 0.05 was considered statistically significant.
| Results | | |
The patients' age, weight, height, BMI, and duration of DPN in the three groups is shown in [Table 1]. There was no statistically significant difference (P > 0.05) between patients in the three groups as regards age, weight, height, BMI, and the duration of DPN. | Table 1: The patients' ages, weight, height, BMI, and duration of diabetic polyneuropathy in groups A, B, and C
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Group A showed a statistically significant difference (P < 0.05) between pretreatment and post-treatment pain intensity using the Mann-Whitney matched pairs test, with 41.67% improvement in pain intensity on the VAS. Group B also showed a highly significant statistical difference between pretreatment and post-treatment pain intensity with 16.7% improvement for both men and women. As for group C, there was no statistically significant improvement in pain intensity in neither men nor women.
There was no significant difference between men and women in any group as regards age, weight, height, BMI, and the duration of DPN, with a nonsignificant difference as regards improvement in pain intensity on the VAS (P > 0.05).
Mean NCV of the medial plantar was reduced for all groups before treatment. There was no statistically significant difference in the paired t-test between pretreatment and post-treatment as regards the medial plantar SCV in any of the groups [Figure 1] and [Table 2],[Table 3] and [Table 4]; nor was there a significant difference among the three groups as regards SCV. | Figure 1: Medial plantar sensory nerve conduction velocity in groups A, B, and C, before and after treatment.
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 | Table 2: Medial plantar sensory nerve conduction velocity, pretreatment and post-treatment in males and females in group A
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 | Table 3: Medial plantar sensory nerve conduction velocity, pretreatment and post-treatment in males and females in group B
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 | Table 4: Medial plantar sensory nerve conduction velocity, pretreatment and post-treatment in males and females in group C
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| Discussion | | |
Type 2 diabetes mellitus is a major public health concern and it is expected to affect an estimated 366 million people worldwide by 2030 [21]. DPN is the most common complication of diabetes as it affects a significant number of patients [11]. The yearly incidence of distal symmetric polyneuropathy in diabetics is ∼2%, and the lifetime incidence of neuropathy has been estimated to be 37-45% for patients with type 2 diabetes. Significant neuropathic pain occurs in 7.5-24% of all patients with diabetes [22],[23].
NCSs are well-established neurophysiologic techniques used to assess the integrity of larger myelinated sensory and motor fibers. Thus, these studies are normal in pure small fiber neuropathies. However, they can clarify if larger sensory and/or motor nerve fibers are concomitantly involved with a small fiber neuropathy [24]. NCS performed at the time of diabetes diagnosis demonstrate that neuropathy is already present in 10-18% of patients [25],[26], and subclinical neuropathy is also present [27], suggesting that peripheral nerve injury occurs at the earliest stages of diabetes, when there is mild glycemic dysregulation.
In the present study, the included patients had a history of diabetes for 10 years, and clinical DPN for 5 years; they were divided randomly into three groups, 20 patients each, with TENS carried out for the patients in group A, aerobic exercise for patients in group B, and only pharmacological therapy for those in group C. Many researchers have considered higher age, low socioeconomic status, treatment with insulin, longer duration of diabetes, and poor glycemic control as risk factors for DPN [28]. Other researchers have stated that the lower limbs are affected first and most severely. Most small fiber neuropathies occur in a length-dependent fashion, resulting in sensory dysfunction in a stocking distribution in the lower extremities. A glove-like loss affects the upper extremities in more advanced cases. Rarely, a non-length-dependent neuropathy, involving the trunk, face, proximal limbs, or other focal areas occur [5],[6]. Many studies reported that the medial plantar sensory NCS provided a more sensitive diagnosis of DPN, even in patients with normal range measurements in the sural nerve [29].
Our patients were assessed before and after 8 weeks of treatment using VAS and medial plantar NCS. Pain intensity decreased significantly by 41.67% in group A, in which patients had received TENS; this is in agreement with the results of other studies [30,31], which compared effect of TENS versus placebo on pain sensitivity. The results showed improvement in sensitivity to pain after TENS. A study by Cheing and Luk [30] assessed the patients on the seventh and fourteenth day of treatment with TENS versus placebo. In their study, Frost et al. [31] evaluated the TENS in comparison with placebo, with skin electrodes placed over the common peroneal nerve, at a low frequency mode (4 Hz) and with the intensity set between 5 and 70 mA; both legs were assessed for at least 5 h/day. After 6 weeks of treatment, significant improvement in intensity of pain was seen on the VAS, which proved that TENS is an effective tool for DPN. The results in this study were also consistent with those of a study by Hamza et al. [19], which used TENS for 30 min, for 3 days a week. Other authors described alteration of pain in a patient with severe DPN, for whom TENS was delivered 1-2 h a day, and through the entire night, through electrodes delivered on the lumbar area. Researchers found that after 20 min of TENS on the first day, the patient reported 38% reduction in the intensity of pain, and after 17 days, the patient reported no pain and comfortable sleep throughout the night.
In the present study, TENS had no significant statistical effect on SCV, which is inconsistent with the results obtained in a study by Alves-Gurrreiro et al. [32]; they examined the effect of three electrotherapeutic modalities, including TENS, on median NCSs, and concluded that TENS had no significant effect on the peripheral nerve conduction, which was in agreement with the results of a study by Sluka et al. [33].
These results are in contradiction with those of a study by Walsh et al. [14], where researchers investigated the effect of four combinations of TENS parameters on nerve conduction velocity NCV parameters and negative peak latency NPL. Their findings revealed that the application of one combination of TENS parameter (100 Hz and 200 ms) directly over the course of the nerve produced a significant increase in NCV and a decrease in NPL.
Predominant or entire damage of the small myelinated A delta fibers or unmyelinated C fibers causes the sense of pain, while NCS assess the integrity of larger myelinated sensory and motor fibers, which explains why NCSs are usually normal in pure small fiber neuropathies [24], given that, patients in this study were diabetics for 10 years, and symptomatic diabetic neuropathy for 5 years, medial plantar SCV was reduced, due to involvement of larger and faster myelinated fibers. SCV showed no significant increase in SCV after treatment with TENS in spite of improvement in neuropathic pain. The contradiction in the effect of TENS on NCV in different studies can be explained by the fact that the suggested mechanism of reduction of neuropathic pain is one of two theories, one of which involves large fibers. The first is the gate control theory of pain, which states that TENS activates the large diameter Aβ and C fibers, and then the large fibers send collaterals to substantia gelatinosa of Rolando, which closes the gate of pain perception to the brain [33]. The second is supraspinal inhibition of pain by endogenous endorphins and enkephalins, which combines with opiate receptors in the periventricular nuclei of the third ventricle and substantia nigra, activating raphe magnus and the reticularis magnocellularis. The descending output releases enkephalins, which inhibits the release of substance P as well as the spinothalamic pain discharge [34].
Group B in the present study significantly improved by 16.7% on VAS after aerobic exercise, which is consistent with the results of several studies showing improvement on VAS scale and delayed development of pain [35],[36],[37],[38]. Exercise in the present study had no significant effect on NCV, which is in agreement with a study by Tesfaye and Boulton [39], who reported significant increase in NCV after exercise in normal subjects. Yet, these results are in disagreement with a study by Fisher et al. [40], who reported a statistically significant improvement in all electrophysiological parameters after exercise, including motor and sensory NCVs and amplitudes, as well as F-wave latencies after a 24-week program. Using deep breathing exercises, combined with gentle aerobic exercises, Hung et al. [41] in their study reported a significant improvement in median and tibial CVs and sensory distal latencies of ulnar nerves.
In conclusion, TENS, of moderate intensity, carried out at 14 Hz, with a pulse width of 250 ms, for 30 min, and three times a week is better than exercise training program in relieving pain in patients with DPN. In contrast, neither TENS nor exercise showed any significant effect on medial plantar CV in patients with DPN.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Deshpande AD, Hayes MH, Schootman M. Epidemiology of diabetes and diabetes-related complications. Phys Ther 2008; 88 :1254-1264.  |
| 2. | Duby JJ, Campbell RK, Setter SM, White JR, Rasmussen KA. Diabetic neuropathy: an intensive review. Am J Health Syst Pharm 2004; 61 :160-167. |
| 3. | Sumner CJ, Sheth S, Griffin JW, Cornblath DR, Polydefkis M. The spectrum of neuropathy in diabetes and impaired glucose tolerance. Neurology 2003; 60 :108-111. |
| 4. | Gibbons CH, Freeman R. Treatment-induced diabetic neuropathy: a reversible painful autonomic neuropathy. Ann Neurol 2010; 67 :534-541. |
| 5. | Tavee J, Zhou L. Small fiber neuropathy: a burning problem. Cleve Clin J Med 2009; 76 :297-305. |
| 6. | Hsieh ST. Pathology and functional diagnosis of small-fiber painful neuropathy. Acta Neurol Taiwan 2010; 19 :82-89. |
| 7. | Bril V, England J, Franklin GM, BackonjaMCohenJDel ToroD, et, al. Evidence-based guideline: treatment of painful diabetic neuropathy: report of the American Academy of Neurology, the American Association of Neuromuscular and Electrodiagnostic Medicine, and the American Academy of Physical Medicine and Rehabilitation. Neurology 2011; 76 : 1758-165. |
| 8. | American Academy of neurology. AAN summary of evidence-based guideline for clinicians. Treatment of painful diabetic neuropathy. Treatment of painful diabetic neuropathy; 2013. Available at: http://www.aan.com. [Last accessed on 2014 Oct]. |
| 9. | Arora N, Niraj G. Management of painful peripheral diabetic neuropathy. BJMP 2013; 6 :606. |
| 10. | Tanenberg RJ. Diabetic peripheral neuropathy: painful or painless. In: Hospital Physician. Greeneville, 2009: 1-8. |
| 11. | Khalil H. Painful diabetic neuropathy management. Int J Evid Based Healthc 2013; 11 :77-79. |
| 12. | Dubinsky M, Miyasaki J. Assessment: efficacy of transcutaneous electric nerve stimulation in treatment of pain in neurologic disorders (an evidence based review): report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Acad Neurol 2009; 74 :1-4. |
| 13. | White P, Craig W, Mdhesham E. Transcutaneous electric nerve stimulation. Diabetes Care 2000; 23 :365-370. |
| 14. | Walsh DM, Lawe AS, Cormack C. Transcutaneous electric nerve stimulation effect on peripheral nerve conduction, mechanical pain threshold and tactile threshold in humans. Arch Phys Med Rehab 2008; 79 :1051-1058. |
| 15. | Anoop M, NK Alappan, Vikram NK, Goel K. Effect of supervised progressive resistance-exercise training protocol on insulin sensitivity, glycemia, lipids, and body composition in Asian islands with type II diabetes. Diabetes Care 2008; 31 :1282-1287. |
| 16. | Carter G. Living with neuropathy. Neurol Now 2007; 3 :33-35. |
| 17. | Said G. Diabetic neuropathy - a review. Nat Clin Pract Neurol 2007; 3 :331-340. |
| 18. | Preston D, Shapiro B. Electromyography and neuromuscular disorders. Philadelphia, Pennsylvania: Elsevier; 2005. 40-43. |
| 19. | Hamza MA, White PE, Craig WF, Ghonarae ES, Ahmed HE, Proctor TJ. Percutaneous electric nerve stimulation: a novel analgesic therapy for diabetic neuropathic pain. Diabetes Care 2000; 23 :365-370. |
| 20. | Sigal RJ, Kenny GP, Wasserman DH, Castane C, White RD. Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care 2006; 29 :1433-1438. |
| 21. | Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diab Care 2004; 27 :1047-1053. |
| 22. | Gaster B, Hirsch IB. The effects of improved glycemic control on complications in type 2 diabetes. Arch Intern Med 1998; 158 :134-140. |
| 23. | Ziegler D. Treatment of diabetic neuropathy and neuropathic pain: how far have we come? Diabetes Care 2008; 31 :255-261. |
| 24. | Hovaguimian A, Gibbons CH. Diagnosis and treatment of pain in small fiber neuropathy. Curr Pain Headache Rep 2011; 15 :193-200. |
| 25. | Lehtinen JM, Niskanen L, Hyvonen K, Siitonen O, Uusitupa M. Nerve function and its determinants in patients with newly-diagnosed type 2 (non-insulin-dependent) diabetes mellitus and in control subjects - a 5-year follow-up. Diabetologia 1993; 36 :68-72. |
| 26. | Cohen JA, Jeffers BW, Faldut D, Marcoux M, Schrier RW. Risks for sensorimotor peripheral neuropathy and autonomic neuropathy in non-insulin-dependent diabetes mellitus (NIDDM) Muscle Nerve 1998; 21 :72-80. |
| 27. | Albers JW, Herman WH, Pop-Busui R, et al. Subclinical neuropathy among diabetes control and complications trial participants without diagnosable neuropathy at trial completion: possible predictors of incident neuropathy? Diab Care 2007; 30 :2613-2618. |
| 28. | Mørkrid K, Ali L, Hussain A. Risk factors and prevalence of diabetic peripheral neuropathy: a study of type 2 diabetic outpatients in Bangladesh. Int J Diabetes Dev Ctries 2010; 30 :11-17. |
| 29. | An JY, Park MS, Kim JS, Shon YM, Lee SJ, Kim YI, et al. Comparison of diabetic neuropathy symptom score and medial plantar sensory nerve conduction studies in diabetic patients showing normal routine nerve conduction studies. Intern Med 2008; 47 :1395-1398. |
| 30. | Cheing G, Luk M. Transcutaneous electric nerve stimulation for neuropathic pain. J Hand Surg Br 2005; 30 :50-55. |
| 31. | Frost T, Nguyen M, Frost S, Disselhoff B, Pohlmann T, Pfutzner A. Impact of low frequency transcutaneous electric nerve stimulation on symptomatic diabetic neuropathy using the new Salutaris device. Diabetes Nutr Metab 2004; 17 :163-168. |
| 32. | Alves-Guerreiro J, Noble JG, Lowe AS, Walsh DM. The effect of three electrotherapeutic modalities upon peripheral nerve conduction and mechanical pain threshold. Clin Physiol 2001; 21 :704-711. |
| 33. | Sluka KA, Walsh D. Transcutaneous electric nerve stimulation for neuropathic: basic science mechanisms and clinical effectiveness. J Pain 2003; 4 :109-121. |
| 34. | Radbakrishnan R, Sluka KA. Spinal muscarinic receptors are activated during low or high frequency TENS induce hyperalgesiaian rats. Neuropharmacology; 45 :1111-1119. |
| 35. | Kluding PM, Pasnoor M, Singh R, Farmer K, et al. The effect of exercise on neuropathic symptoms, nerve function, and cutaneous innervations in people with diabetic peripheral neuropathy. J Diabetes Complications 2012; 26 :424-429. |
| 36. | Balducci S, Iacobellis GT, Parisi L. Exercise training can modify the natural history of diabetic peripheral neuropathy. J Diabetes Complications 2006; 20 :216-223. |
| 37. | Smith AG, Russell J, Peltier A. Lifestyle intervention for prediabetic neuropathy. Diabetes Care 29 :1294-1299. |
| 38. | Sahadev A, Erika S, Evan B. Forced-exercise delays neuropathic pain in experimental diabetes: effects on voltage-activated calcium channels. J Neurochem 2011; 118 :224-236. |
| 39. | Tesfaye S, Boulton AJM, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. On Behalf of the Toronto Diabetic Neuropathy Criteria Group. Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 2010; 33 :2725-2793. |
| 40. | Fisher MA, Langbein WE, Collins EG, Corzine L. Physiological improvement with moderate exercise in type 2 diabetic neuropathy. Electromyogr Clin Neurophysiol 2007; 47 :23-28. |
| 41. | Hung J, Liou C, Wang P. The effect of Tai Chi chuan exercise on peripheral nerve modulation in patients with type 2 diabetes mellitus in women. N Engl J Med 2009; 345 :790-797. |
[Figure 1]
[Table 1], [Table 2], [Table 3], [Table 4]
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