http://informahealthcare.com/ptp ISSN: 0959-3985 (print), 1532-5040 (electronic) Physiother Theory Pract, Early Online: 1–5 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/09593985.2014.903547
RESEARCH REPORT
The effects of transcutaneous electrical nerve stimulation on joint position sense in patients with knee joint osteoarthritis
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Zahra Rojhani Shirazi, PT, PhD, Razieh Shafaee, PT, BSc, and Leila Abbasi, PT, BSc, PhD Candidate School of Rehabilitation Sciences, Shiraz University of Medical Sciences, Shiraz, Iran
Abstract
Keywords
Objective: To study the effects of transcutaneous electrical nerve stimulation (TENS) on joint position sense (JPS) in knee osteoarthritis (OA) subjects. Methods: Thirty subjects with knee OA (40–60 years old) using non-random sampling participated in this study. In order to evaluate the absolute error of repositioning of the knee joint, Qualysis Track Manager system was used and sensory electrical stimulation was applied through the TENS device. Results: The mean errors in repositioning of the joint, in two position of the knee joint with 20 and 60 degree angle, after applying the TENS was significantly decreased (p50.05). Conclusion: Application of TENS in subjects with knee OA could improve JPS in these subjects.
Knee osteoarthritis, joint position sense, transcutaneous electrical nerve stimulation
Introduction Osteoarthritis (OA) is a common joint disorder characterized by pain, inability to climb stairs, increased pain with exercise, giving way during walking, varus deformity and decreased balance. The most common joint affected by degeneration, especially in older ages, is the knee (Baliunas et al, 2002; Felson and Zhang, 1998; Kirkley et al, 1999). Disorders of proprioception, balance and muscle coordination often lead to knee joint instability. Furthermore, pain causes weakness and inhibits muscle function (Heiden, Lloyd, and Ackland, 2009; Hortoba´gyi et al, 2005). Another symptom of knee OA is joint swelling, which can lead to muscle weakness and affect proprioception (Bopf et al, 2010; Devanne and Maton, 1998; Knoop et al, 2011). Proprioception is often defined as a conscious and/or unconscious perception of position and movement of an extremity or a joint in space (Collins et al, 2011; Grob et al, 2002; Hurley, Scott, Rees, and Newham, 1997; Sharma, 1999). Knee proprioception derives from the integration of afferent signals from proprioceptive receptors in different structures of the knee and is influenced by signals from outside the knee (e.g. from the vestibular organs, visual system and cutaneous and proprioceptive receptors from other body parts) (Lephart, Pincivero, Giraido, and Fu, 1997; Sharma, 1999; Solomonow and D’Ambrosia, 1991). Various methods for measuring proprioceptive accuracy of the knee have been described. One of the tests that measures knee proprioception is the position sense test in which the knee is moved (actively or passively) toward a criterion angle. After a few seconds, the knee is returned to the original position. Following this, the subject has to reproduce the perceived angle (Barrett, Cobb, and Bentley, 1991; Bennell et al, 2003; Lund et al, 2008). A second test measures the sensations of passive, slow knee motions (motion sense tests or threshold detection tests) Address correspondence to Leila Abbasi, School of Rehabilitation Sciences, Shiraz University of Medical Sciences, Shiraz, Iran. E-mail: [email protected]
History Received 20 August 2013 Revised 6 February 2014 Accepted 11 February 2014 Published online 3 April 2014
(Pai, Rymer, Chang, and Sharma, 1997; Sharma, Pai, Holtkamp, and Rymer, 1997). Many of the current treatments for knee OA focus on symptom modification and there is a great clinical need for a disease-modifying treatment in order to reduce healthcare costs and improve the quality of life. One potential means of further enhancing the improvement in proprioception is subsensory stochastic resonance (SR) electrical stimulation. SR stimulation is a type of electrical or mechanical stimulation with an alternating electric field that, at a subsensory level, has been shown to enhance the detection and transmission of weak sensory signals (Collins, Imhoff, and Grigg, 1996; Cordo et al, 1996). SR is thought to alter the transmembrane potential of neurons, causing the cell to depolarize and making it more likely that an action potential will result (Collins et al, 2011). SR has shown promise in improving balance in various populations including the following: the elderly (Dhruv et al, 2002; Gravelle et al, 2002); those with diabetic neuropathy (Hijmans et al, 2008); and those recovering from stroke (Priplata et al, 2006). As somatosensory feedback is an important component to the balance control system, it has been theorized that the improved balance observed with SR stimulation is a result of enhanced proprioceptive input (Gravelle et al, 2002). Gravelle et al (2002) tested the effect of SR with low-level electrical noise, applied at the knee, on balance control in healthy elderly volunteers. They showed that low-level input noise (electrical or mechanical) can enhance the sensitivity of the human somatosensory system. The results suggested that imperceptible electrical noise, when applied to the knee, can enhance the balance performance of healthy older adults. Dhruv et al (2002) showed that low-level electrical noise could significantly improve fine-touch sensitivity on the plantar surface of the foot in the elderly using Semmes-Weinstein monofilaments. Their study suggested that electrical noise-based techniques may enable people to overcome functional difficulties due to agerelated sensory loss. Transcutaneous electrical nerve stimulation (TENS) is a non invasive modality with very few adverse effects that frequently is
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
2
Z. R. Shirazi et al.
used in physiotherapy for pain control (Osiri et al, 2009). TENS has the advantage of being efficacious, inexpensive, simple and essentially free of side effects. TENS may even be used at home by subjects themselves due to its portability and simplicity (Itoh et al, 2008). TENS can be set to different frequencies, durations and intensities. This results in a large recruitment of sensory nerve fibers and mechanoreceptors (Sluka and Walsh, 2003). Different types of TENS treatment are often referred to as Hi-TENS and Low-TENS. The high frequency TENS or conventional TENS with 40–120 Hz frequency temporarily reduces the cutaneous (skin) perception for touch by increasing the sensory threshold in the area. The low frequency TENS is applied at frequencies from two to four HZ and generates muscle contractions (Mima et al, 2004). Therefore, TENS usually is used with sensory threshold or supra-threshold amplitude compare with sub-threshold sensorimotor signals of SR. TENS seems to be more acceptable than SR stimulation among subjects because of its perceptible stimulation current, but its effect on proprioception is unknown. Several investigations on the effects of SR have reported improvements in balance control when an electrical or mechanical noise was applied (Gravelle et al, 2002; Priplata et al, 2002, 2006). Moreover, Dickstein, Laufer, and Katz (2006) showed that an intervention of high frequency TENS to the lower leg had a positive effect on postural sway, suggesting that the electrical input contributes to a decrease in the mechanoreceptor threshold, responsible for proprioceptive detection (i.e. improved proprioception sense) (Dickstein, Laufer, and Katz, 2006). None of the previous investigations had examined the possible effect on proprioception sense after the electrical intervention. It should be noted that past SR stimulation studies have demonstrated an optimal stimulation level for increasing the sensitivity of somatosensory receptors to mechanical stimuli, and that stimulation outside of this optimal range may have little effect (Collins, Imhoff, and Grigg, 1996; Cordo et al, 1996); but Collins et al (2011) observed the fact that an improvement in joint position sense (JPS) was not seen during both of the stimulation conditions (E50/S and E75/S) compared to the sleeve alone condition and concluded it may be a result of an inadequate stimulation amplitude. Thus, according to the electrical nature of TENS and capability of electrical noise to improve proprioception in addition to control of the reflex function, we hypothesized that the knee JPS of subjects with knee OA would be improved, and joint repositioning error would be reduced with the application of transcutaneous electrical stimulation with sensory threshold amplitude.
Materials and methods
Physiother Theory Pract, Early Online: 1–5
sufficiently activate the muscle spindles and mechanoreceptors necessary for improvements in JPS (Collins et al, 2011). Inclusion criteria were aged more than 40 years; radiographic evidence of knee OA; and a physician’s confirmation. The medial and lateral compartments of the joint were both assessed to ensure greater narrowing on the medial side. All subjects had moderate pain about 3–6 in numeric rating scale where 0 represents ‘‘no pain’’ and 10 represents ‘‘the worst pain possible’’ (Hartrick, Kovan, and Shapiro, 2003). During testing, the subject’s more severely affected knee joint was chosen for testing, but in instances where both knees were equally affected, the subject’s dominant knee was tested. Exclusion criteria were as follows: any neurological impairment that disturbed the sense of pain; pacemaker or any other implantable electronic device; musculoskeletal disease; joint replacement within the tested lower extremity; rheumatoid or other systemic inflammatory arthritis; pregnancy; and body mass index more than 35. Procedures After a visit and assessment of the inclusion criteria, the subjects signed consent forms and then participated in the study. To measure the error in repositioning of the joint angle, the participant sat on a chair as shown in Figure 1, the infrared markers were attached on the greater trochanter, medial and lateral femoral condyle and medial and lateral malleoli. In addition, two cluster markers were attached on the femur and on the leg. Primary position of the knee was 90-degree flexion; then, the subjects were requested to move their leg toward extension to test angle (20 or 60 degrees) with extension angle monitoring via motion analyzer cameras. We determined the joint angles to be tested according to previous studies (Baker et al, 2002; Bennell et al, 2005). Subjects were then asked to hold this position for 5 s. After that, they were instructed to return to the primary position. Following a 5-s rest period, they were requested to assume the previous angle and hold for 3 s. The difference between these two attempts was used to establish the target angle and defined as repositioning error before the treatment condition. The cameras of the motion analysis system (Qualysis, Gothenburg, Sweden) captured the test process. During testing, subjects wore a blindfold in order to eliminate visual cues. The test was repeated three times, and the average was considered for statistical analysis. The selection order of the test angles was random. This procedure was done before and immediately after the use of electrical stimulation applied via an electrical stimulator device (conventional TENS with the duration of 50 ms and 100 HZ frequency) through pairs of electrodes (Mascarin et al, 2012) placed on the medial and lateral joint line of the knee for 5 min. Finally, the absolute repositioning error before and after TENS application condition was measured.
Participants Thirty female subjects with minimal to moderate (Grades 1–3) medial compartment knee OA were recruited in the study. Women are more severely and more frequently affected by knee OA. Differences in knee anatomy, kinematics, previous knee injury and hormonal influences may play a role (Hame and Alexander, 2013). Therefore, we recruited just female subjects to eliminating intersubject differences. The grade of knee OA was assessed by using the modified Kellgren/Lawrence grading system. Subjects were included in the study if they had a diagnosis of medial compartment knee OA confirmed by a physician and if they demonstrated radiographic evidence of knee OA. All recruited subjects selected were referred to the physical therapy clinic of Shiraz Rehabilitation School. Subjects with severe KL grades were not recruited because it is unclear whether the stimulation applied would adequately penetrate the tissue around the knee and
Figure 1. V3D knee model.
Effects of TENS on joint position sense OA subjects
DOI: 10.3109/09593985.2014.903547
Initially, each subject’s threshold for detection of the stimulation was determined by applying the stimulation and incrementally increasing the amplitude until the subject indicated they detected the stimulation. The intensity was monitored throughout the period and turned up, if necessary, to maintain the specified level of the subject’s verbal report.
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Statistical analysis All statistical analyses were performed using SPSS 15 software (SPSS Inc., Chicago, IL). Normality distribution of the variables was checked by One-Sample Kolmogorov–Smirnov test. Descriptive statistics were calculated. To compare mean errors in joint re-positioning between angles (20 and 60 degrees) before and after electrical stimulation, paired t tests were employed. To compare the effect of electrical stimulation on JPS for both angles, independent sample t tests were performed for each angle tested. Pearson correlation was used to determine the relationship between the absolute error (degrees) of the subjects before TENS treatment and the improvement in absolute error seen in the condition for 60 degree angle repositioning.
Results Thirty subjects (40–60 years) with minimal to moderate medial knee OA were studied. The mean age and BMI of these participants were 51.1 (±7.45) years and 26.46 (±3.3), respectively (Table 1). Our population presented with Kellgren– Lawrence grades ranging from 1 to 3, were considered to be mild to moderately functionally impaired and were not excessively obese or elderly. The differences (mean errors) in the knee joint repositioning for both angles (20 and 60 degrees) were reduced significantly after applying sensory electrical stimulation (Table 2). The differences (mean errors) in 20 degrees, before application of sensory electrical stimulation, were significantly less than that in 60 degrees. However, after the application of sensory electrical stimulation, this difference in the mean error was not statistically significant (Table 2). Correlation analysis demonstrated a moderate to strong correlation between the absolute repositioning error before TENS treatment condition and the improvement seen in the absolute error with the TENS treatment condition for both angles of 20 degrees (R ¼ 0.646; p50.005) and angle of 60 degrees (R ¼ 0.555; p50.005; Figure 2).
Table 1. Mean (±SD) demographic information for all test subjects.
Age (years) Height (cm) Weight (kg) BMI (kg/m2) KL grade (1–3) Pain
Upper
Lower
Mean ± SD
60 165 80 33.6 1 6
40 141 55 21.0 3 3
51.1 ± 7.5 155.6 ± 6.3 63.8 ± 6.8 26.5 ± 3.3 2.1 ± 0.6 4.3 ± 0.9
Table 2. Differences (degrees) between the knee joint angle before and after application of sensory electrical stimulation. Before stimulation After stimulation In 20 degree position In 60 degree position
3.2 ± 5.2 4.4 ± 7.7 p ¼ 0.023
1.9 ± 2.4 3.0 ± 3.4 p ¼ 0.304
p ¼ 0.001 p ¼ 0.001
3
Discussion Our study was designed to examine whether TENS is effective on improving proprioception. Repositioning error was used as a criterion to for JPS and somewhat for proprioception (Newcomer et al, 2000). Proprioception can be measured in several different ways. In this study, we used JPS as a measure of proprioception. The results indicate that conventional TENS affects proprioception sense as measured by JPS. The results confirmed that repositioning error on a dynamic position sense task changes with TENS application. The findings of this study demonstrated that the mean of joint repositioning error in both 20 and 60 degrees reduced significantly after applying sensory electrical stimulation. The result of this study is comparable with that of Collins et al (2011). Collins et al (2011) also observed improvements in JPS followed by application of sensory electrical stimulation. In another study, Gravelle et al (2002) observed improvement in the sensitivity of the somatosensory system and balance in older people following electrical stimulation. They indicated improvement in balance because of improvement in proprioception. Gravelle et al (2002) ascribed this finding to small changes in receptor transmembrane potentials that were followed by application of electrical stimulation; this small change in the potential brings the neuron closer to the threshold and increases the possibility of action potential in response to weak signals. Birmingham et al (2001) also noted that the poorer the proprioceptive ability, the greater the improvement after application of an external stimulus. Since proprioception is mediated by afferent input from articular, muscular and cutaneous structures, the improvement in knee joint proprioception was likely due to increased afferent input. The afferent input was increased via enhancement of cutaneous stimulation, muscle spindle and Ruffini receptors, which are located in the ACL from an electrical stimulation; this explanation has also been proposed by others (Barrett, Cobb, and Bentley, 1991). The substantia gelatinosa (SG) cells in the dorsal horn receive afference from ‘‘pain’’ fibers (Ad-fibers and C-fibers), and is believed to modulate the synaptic transmission of nerve impulses from peripheral sensory and nociceptive fibers, to central cells. The gate control theory suggests that afference from large diameter sensory fibers facilitates the inhibitory cells of the SG that in turn block both sensory and nociceptive afference to the central transmission cells, which in turn relay to higher central nervous centers. The central transmission cell is inhibited, or in other words, the ‘‘gate’’ is closed causing not only subjective pain relief but also some reduction in sensory afference to higher centers. The effects of some rehabilitative therapies have been investigated on proprioception improvement including: massage therapy (Henriksen et al, 2004); muscle strengthening (Beard, Dodd, Trundle, and Simpson, 1994); and taping and bracing (Heit, Lephart, and Rozzi, 1996). Henriksen et al (2004) investigated the effects of stimulating massage on intra-individual error in relation to the repeating measurements of JPS, concluding that massage could be a treatment of choice in order to help subjects with reduced JPS following musculoskeletal or neurological pathologies. However, not all rehabilitation modalities studied so far have demonstrated positive effects on JPS. Callaghan, Selfe, Bagley, and Oldham (2002) investigated the effects of patellar taping on proprioception, finding that normal subjects with good proprioception did not benefit from patellar taping, and the authors justified that probably because the data from the good and poor groups canceled out (Callaghan, Selfe, Bagley, and Oldham, 2002). Lund et al (2009) found that massage had no effect on the immediate joint repositioning error in subjects with knee OA, and they concluded that maybe joint
4
Z. R. Shirazi et al.
Physiother Theory Pract, Early Online: 1–5
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Figure 2. The relationship between the absolute error (degrees) of the subjects before TENS treatment and the improvement in absolute error seen in the condition for 60 degree angle repositioning.
repositioning error is not sufficiently sensitive to identify possible effects of massage on proprioception. Moreover, the results of this study showed that before application of TENS, the error size in 60 degrees was significantly less than that in 20 degrees. After applying TENS, the mean errors reduced between two angle positions, but this difference was not significant. This can indicate that TENS could affect proprioceptive receptors in both positions and increase their sensitivity. Our findings also suggest that the transcutaneous electrical stimulation may be most beneficial to apply in subjects with larger proprioceptive deficits. The sensory electrical stimulation used in this study is probably effective in enhancing the function of the human sensorimotor system because of the electrical nature of information transfer in the sensory neurons (Collins et al, 2011). A somatosensory feedback is an essential part of the proprioceptive system (Collins et al, 2011). Therefore, improvement in this sense following the use of TENS increases the sensory afferents. While this study is novel, it has several limitations such as lack of control group and lack of investigation of other sensory amplitude levels.
Conclusion The aim of our study was to determine if TENS might improve JPS. There was significant difference in the JPS before and after TENS treatment. Conventional TENS with sensory threshold amplitude seems to have positive impact on proprioception sense in the knee joint as measured by JPS in subjects with knee OA. Our findings suggest that TENS may be most beneficial to apply in subjects with larger proprioceptive deficits. Future work is necessary to determine if applying different types of TENS with different amplitudes will improve knee proprioception. Further investigations in larger populations and with a well-defined RCT design are needed in subjects with known proprioceptive deficiencies.
Acknowledgements We would like to thank the subjects who participated in the study and also Dr. Nasrin Shokrpour at the Center for Development of Clinical Research of Nemazee Hospital for editorial assistance. This study is extracted from the proposal number 5683 and R. Shafaei’s MSc Thesis.
Declaration of interest The authors report no declarations of interest. This work was financially supported by Shiraz University of Medical Sciences.
References Baker V, Bennell K, Stillman B, Cowan S, Crossley K 2002 Abnormal knee joint position sense in individuals with patellofemoral pain syndrome. Journal of Orthopaedic Research 20: 208–214. Baliunas A, Hurwitz D, Ryals A, Karrar A, Case J, Block J, Andriacchi T 2002 Increased knee joint loads during walking are present in subjects with knee osteoarthritis. Osteoarthritis and Cartilage 10: 573–579. Barrett DS, Cobb AG, Bentley G 1991 Joint proprioception in normal, osteoarthritic and replaced knees. Journal of Bone and Joint Surgery (Br) 73: 53–56. Beard DJ, Dodd CA, Trundle HR, Simpson AH 1994 Proprioception enhancement for anterior cruciate ligament deficiency. A prospective randomised trial of two physiotherapy regimes. Journal of Bone and Joint Surgery (Br) 76: 654–659. Bennell KL, Wee E, Crossley K, Stillman B, Hodges P 2005 Effects of experimentally-induced anterior knee pain on knee joint position sense in healthy individuals. Journal of Orthopaedic Research 23: 46–53. Bennell KL, Hinman RS, Metcalf BR, Crossley KM, Buchbinder R, Smith M, McColl G 2003 Relationship of knee joint proprioception to pain and disability in individuals with knee osteoarthritis. Journal of Orthopaedic Research 21: 792–797. Birmingham T, Kramer J, Kirkley A, Inglis J, Spaulding S, Vandervoort A 2001 Knee bracing for medial compartment osteoarthritis: Effects on proprioception and postural control. Rheumatology 40: 285–289.
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
DOI: 10.3109/09593985.2014.903547
Bopf D, McAuliffe M, Shillington M, Drynan D, Bucknell E 2010 Knee osteoarthritis: Use of investigations and non-operative management in the Australian primary care setting. Australasian Medical Journal 1: 194–197. Callaghan MJ, Selfe J, Bagley PJ, Oldham JA 2002 The effects of patellar taping on knee joint proprioception. Journal of Athletic Training 37: 19–24. Collins AT, Blackburn JT, Olcott CW, Miles J, Jordan J, Dirschl DR, Weinhold PS 2011 Stochastic resonance electrical stimulation to improve proprioception in knee osteoarthritis. Knee 18: 317–322. Collins JJ, Imhoff TT, Grigg P 1996 Noise-enhanced tactile sensation. Nature 383: 770. Cordo P, Inglis JT, Verschueren S, Collins JJ, Merfeld DM, Rosenblum S, Buckley S, Moss F 1996 Noise in human muscle spindles. Nature 383: 769–770. Devanne H, Maton B 1998 Role of proprioceptive information in the temporal coordination between joints. Experimental Brain Research 119: 58–64. Dhruv NT, Niemi JB, Harry JD, Lipsitz LA, Collins JJ 2002 Enhancing tactile sensation in older adults with electrical noise stimulation. Neuroreport 13: 597–600. Dickstein R, Laufer Y, Katz M 2006 TENS to the posterior aspect of the legs decreases postural sway during stance. Neuroscience Letters 393: 51–55. Felson DT, Zhang Y 1998 An update on the epidemiology of knee and hip osteoarthritis with a view to prevention. Arthritis and Rheumatism 41: 1343–1355. Gravelle DC, Laughton CA, Dhruv NT, Katdare KD, Niemi JB, Lipsitz LA, Collins JJ 2002 Noise-enhanced balance control in older adults. Neuroreport 13: 1853–1856. Grob K, Kuster M, Higgins S, Lloyd D, Yata H 2002 Lack of correlation between different measurements of proprioception in the knee. Journal of Bone and Joint Surgery (Br) 84: 614–618. Hame SL, Alexander RA 2013 Knee osteoarthritis in women. Current Reviews in Musculoskeletal Medicine 6: 182–187. Hartrick CT, Kovan JP, Shapiro S 2003 The numeric rating scale for clinical pain measurement: A ratio measure? Pain Practice 3: 310–316. Heiden TL, Lloyd DG, Ackland TR 2009 Knee joint kinematics, kinetics and muscle co-contraction in knee osteoarthritis patient gait. Clinical Biomechanics 24: 833–841. Heit EJ, Lephart SM, Rozzi SL 1996 The effect of ankle bracing and taping on joint position sense in the stable ankle. Journal of Sport Rehabilitation 5: 206–213. Henriksen M, Højrup A, Lund H, Christensen L, Danneskiold-Samsøe B, Bliddal H 2004 The effect of stimulating massage of thigh muscles on knee joint position sense. Advances in Physiotherapy 6: 29–36. Hijmans JM, Geertzen JHB, Zijlstra W, Hof AL, Postema K 2008 Effects of vibrating insoles on standing balance in diabetic neuropathy. Journal of Rehabilitative Research and Development 45: 1441–1450. Hortoba´gyi T, Westerkamp L, Beam S, Moody J, Garry J, Holbert D, DeVita P 2005 Altered hamstring-quadriceps muscle balance in subjects with knee osteoarthritis. Clinical Biomechanics 20: 97–104. Hurley MV, Scott DL, Rees J, Newham DJ 1997 Sensorimotor changes and functional performance in subjects with knee osteoarthritis. Annals of the Rheumatic Diseases 56: 641–648. Itoh K, Hirota S, Katsumi Y, Ochi H, Kitakoji H 2008 A pilot study on using acupuncture and transcutaneous electrical nerve stimulation
Effects of TENS on joint position sense OA subjects
5
(TENS) to treat knee osteoarthritis (OA). Chinese Medicine 3: 2. doi: 10.1186/1749-8546-3-2. Kirkley A, Webster-Bogaert S, Litchfield R, Amendola A, MacDonald S, McCalden R, Fowler P 1999 The effect of bracing on varus gonarthrosis. Journal of Bone and Joint Surgery (Am) 81: 539–548. Knoop J, Steultjens M, van der Leeden M, van der Esch M, Thorstensson C, Roorda L, Lems W, Dekker J 2011 Proprioception in knee osteoarthritis: A narrative review. Osteoarthritis and Cartilage 19: 381–388. Lephart SM, Pincivero D, Giraido J, Fu FH 1997 The role of proprioception in the management and rehabilitation of athletic injuries. American Journal of Sports Medicine 25: 130–137. Lund H, Henriksen M, Bartels EM, Danneskiold-Samsøe B, Bliddal H 2009 Can stimulating massage improve joint repositioning error in subjects with knee osteoarthritis? Journal of Geriatric Physical Therapy 32: 111–116. Lund H, Juul-Kristensen B, Hansen K, Christensen R, Christensen H, Danneskiold-Samsøe B, Bliddal H 2008 Movement detection impaired in subjects with knee osteoarthritis compared to healthy controls: A cross-sectional case-control study. Journal of Musculoskeletal and Neuronal Interactions 8: 391–400. Mascarin N, Vancini R, dos Andrade M, de Magalha˜es E, de Lira CA, Coimbra I 2012 Effects of kinesiotherapy, ultrasound and electrotherapy in management of bilateral knee osteoarthritis: Prospective clinical trial. BMC Musculoskeletal Disorders 13: 182–190. Mima T, Oga T, Rothwell J, Satow T, Yamamoto J-i, Toma K, Fukuyama H, Shibasaki H, Nagamine T 2004 Short-term high-frequency transcutaneous electrical nerve stimulation decreases human motor cortex excitability. Neuroscience Letters 355: 85–88. Newcomer KL, Laskowski ER, Yu B, Johnson JC, An KN 2000 Differences in repositioning error among subjects with low back pain compared with control subjects. Spine 25: 2488–2493. Osiri M, Welch V, Brosseau L, Shea B, McGowan J, Tugwell P, Wells G 2009 Transcutaneous electrical nerve stimulation for knee osteoarthritis. Cochrane Database of Systematic Reviews 4: CD002823. Pai YC, Rymer WZ, Chang RW, Sharma L 1997 Effect of age and osteoarthritis on knee proprioception. Arthritis and Rheumatism 40: 2260–2265. Priplata A, Niemi J, Salen M, Harry J, Lipsitz LA, Collins J 2002 Noiseenhanced human balance control. Physical Review Letters 89: 238101– 238104. Priplata AA, Patritti BL, Niemi JB, Hughes R, Gravelle DC, Lipsitz LA, Veves A, Stein J, Bonato P, Collins JJ 2006 Noise-enhanced balance control in subjects with diabetes and subjects with stroke. Annals of Neurology 59: 4–12. Sharma L 1999 Proprioceptive impairment in knee osteoarthritis. Rheumatic Diseases Clinics of North America 25: 299–314. Sharma L, Pai YC, Holtkamp K, Rymer WZ 1997 Is knee joint proprioception worse in the arthritic knee versus the unaffected knee in unilateral knee osteoarthritis? Arthritis and Rheumatism 40: 1518–1525. Sluka KA, Walsh D 2003 Transcutaneous electrical nerve stimulation: Basic science mechanisms and clinical effectiveness. Journal of Pain 4: 109–121. Solomonow M, D’Ambrosia R 1991 Neural reflex arcs and muscle control of knee stability and motion. In: Scott WN (ed) Ligament and extensor mechanism injuries of the knee, pp 389–400. St. Louis, Mosby Year Book.
RESEARCH REPORT
The effects of transcutaneous electrical nerve stimulation on joint position sense in patients with knee joint osteoarthritis
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Zahra Rojhani Shirazi, PT, PhD, Razieh Shafaee, PT, BSc, and Leila Abbasi, PT, BSc, PhD Candidate School of Rehabilitation Sciences, Shiraz University of Medical Sciences, Shiraz, Iran
Abstract
Keywords
Objective: To study the effects of transcutaneous electrical nerve stimulation (TENS) on joint position sense (JPS) in knee osteoarthritis (OA) subjects. Methods: Thirty subjects with knee OA (40–60 years old) using non-random sampling participated in this study. In order to evaluate the absolute error of repositioning of the knee joint, Qualysis Track Manager system was used and sensory electrical stimulation was applied through the TENS device. Results: The mean errors in repositioning of the joint, in two position of the knee joint with 20 and 60 degree angle, after applying the TENS was significantly decreased (p50.05). Conclusion: Application of TENS in subjects with knee OA could improve JPS in these subjects.
Knee osteoarthritis, joint position sense, transcutaneous electrical nerve stimulation
Introduction Osteoarthritis (OA) is a common joint disorder characterized by pain, inability to climb stairs, increased pain with exercise, giving way during walking, varus deformity and decreased balance. The most common joint affected by degeneration, especially in older ages, is the knee (Baliunas et al, 2002; Felson and Zhang, 1998; Kirkley et al, 1999). Disorders of proprioception, balance and muscle coordination often lead to knee joint instability. Furthermore, pain causes weakness and inhibits muscle function (Heiden, Lloyd, and Ackland, 2009; Hortoba´gyi et al, 2005). Another symptom of knee OA is joint swelling, which can lead to muscle weakness and affect proprioception (Bopf et al, 2010; Devanne and Maton, 1998; Knoop et al, 2011). Proprioception is often defined as a conscious and/or unconscious perception of position and movement of an extremity or a joint in space (Collins et al, 2011; Grob et al, 2002; Hurley, Scott, Rees, and Newham, 1997; Sharma, 1999). Knee proprioception derives from the integration of afferent signals from proprioceptive receptors in different structures of the knee and is influenced by signals from outside the knee (e.g. from the vestibular organs, visual system and cutaneous and proprioceptive receptors from other body parts) (Lephart, Pincivero, Giraido, and Fu, 1997; Sharma, 1999; Solomonow and D’Ambrosia, 1991). Various methods for measuring proprioceptive accuracy of the knee have been described. One of the tests that measures knee proprioception is the position sense test in which the knee is moved (actively or passively) toward a criterion angle. After a few seconds, the knee is returned to the original position. Following this, the subject has to reproduce the perceived angle (Barrett, Cobb, and Bentley, 1991; Bennell et al, 2003; Lund et al, 2008). A second test measures the sensations of passive, slow knee motions (motion sense tests or threshold detection tests) Address correspondence to Leila Abbasi, School of Rehabilitation Sciences, Shiraz University of Medical Sciences, Shiraz, Iran. E-mail: [email protected]
History Received 20 August 2013 Revised 6 February 2014 Accepted 11 February 2014 Published online 3 April 2014
(Pai, Rymer, Chang, and Sharma, 1997; Sharma, Pai, Holtkamp, and Rymer, 1997). Many of the current treatments for knee OA focus on symptom modification and there is a great clinical need for a disease-modifying treatment in order to reduce healthcare costs and improve the quality of life. One potential means of further enhancing the improvement in proprioception is subsensory stochastic resonance (SR) electrical stimulation. SR stimulation is a type of electrical or mechanical stimulation with an alternating electric field that, at a subsensory level, has been shown to enhance the detection and transmission of weak sensory signals (Collins, Imhoff, and Grigg, 1996; Cordo et al, 1996). SR is thought to alter the transmembrane potential of neurons, causing the cell to depolarize and making it more likely that an action potential will result (Collins et al, 2011). SR has shown promise in improving balance in various populations including the following: the elderly (Dhruv et al, 2002; Gravelle et al, 2002); those with diabetic neuropathy (Hijmans et al, 2008); and those recovering from stroke (Priplata et al, 2006). As somatosensory feedback is an important component to the balance control system, it has been theorized that the improved balance observed with SR stimulation is a result of enhanced proprioceptive input (Gravelle et al, 2002). Gravelle et al (2002) tested the effect of SR with low-level electrical noise, applied at the knee, on balance control in healthy elderly volunteers. They showed that low-level input noise (electrical or mechanical) can enhance the sensitivity of the human somatosensory system. The results suggested that imperceptible electrical noise, when applied to the knee, can enhance the balance performance of healthy older adults. Dhruv et al (2002) showed that low-level electrical noise could significantly improve fine-touch sensitivity on the plantar surface of the foot in the elderly using Semmes-Weinstein monofilaments. Their study suggested that electrical noise-based techniques may enable people to overcome functional difficulties due to agerelated sensory loss. Transcutaneous electrical nerve stimulation (TENS) is a non invasive modality with very few adverse effects that frequently is
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
2
Z. R. Shirazi et al.
used in physiotherapy for pain control (Osiri et al, 2009). TENS has the advantage of being efficacious, inexpensive, simple and essentially free of side effects. TENS may even be used at home by subjects themselves due to its portability and simplicity (Itoh et al, 2008). TENS can be set to different frequencies, durations and intensities. This results in a large recruitment of sensory nerve fibers and mechanoreceptors (Sluka and Walsh, 2003). Different types of TENS treatment are often referred to as Hi-TENS and Low-TENS. The high frequency TENS or conventional TENS with 40–120 Hz frequency temporarily reduces the cutaneous (skin) perception for touch by increasing the sensory threshold in the area. The low frequency TENS is applied at frequencies from two to four HZ and generates muscle contractions (Mima et al, 2004). Therefore, TENS usually is used with sensory threshold or supra-threshold amplitude compare with sub-threshold sensorimotor signals of SR. TENS seems to be more acceptable than SR stimulation among subjects because of its perceptible stimulation current, but its effect on proprioception is unknown. Several investigations on the effects of SR have reported improvements in balance control when an electrical or mechanical noise was applied (Gravelle et al, 2002; Priplata et al, 2002, 2006). Moreover, Dickstein, Laufer, and Katz (2006) showed that an intervention of high frequency TENS to the lower leg had a positive effect on postural sway, suggesting that the electrical input contributes to a decrease in the mechanoreceptor threshold, responsible for proprioceptive detection (i.e. improved proprioception sense) (Dickstein, Laufer, and Katz, 2006). None of the previous investigations had examined the possible effect on proprioception sense after the electrical intervention. It should be noted that past SR stimulation studies have demonstrated an optimal stimulation level for increasing the sensitivity of somatosensory receptors to mechanical stimuli, and that stimulation outside of this optimal range may have little effect (Collins, Imhoff, and Grigg, 1996; Cordo et al, 1996); but Collins et al (2011) observed the fact that an improvement in joint position sense (JPS) was not seen during both of the stimulation conditions (E50/S and E75/S) compared to the sleeve alone condition and concluded it may be a result of an inadequate stimulation amplitude. Thus, according to the electrical nature of TENS and capability of electrical noise to improve proprioception in addition to control of the reflex function, we hypothesized that the knee JPS of subjects with knee OA would be improved, and joint repositioning error would be reduced with the application of transcutaneous electrical stimulation with sensory threshold amplitude.
Materials and methods
Physiother Theory Pract, Early Online: 1–5
sufficiently activate the muscle spindles and mechanoreceptors necessary for improvements in JPS (Collins et al, 2011). Inclusion criteria were aged more than 40 years; radiographic evidence of knee OA; and a physician’s confirmation. The medial and lateral compartments of the joint were both assessed to ensure greater narrowing on the medial side. All subjects had moderate pain about 3–6 in numeric rating scale where 0 represents ‘‘no pain’’ and 10 represents ‘‘the worst pain possible’’ (Hartrick, Kovan, and Shapiro, 2003). During testing, the subject’s more severely affected knee joint was chosen for testing, but in instances where both knees were equally affected, the subject’s dominant knee was tested. Exclusion criteria were as follows: any neurological impairment that disturbed the sense of pain; pacemaker or any other implantable electronic device; musculoskeletal disease; joint replacement within the tested lower extremity; rheumatoid or other systemic inflammatory arthritis; pregnancy; and body mass index more than 35. Procedures After a visit and assessment of the inclusion criteria, the subjects signed consent forms and then participated in the study. To measure the error in repositioning of the joint angle, the participant sat on a chair as shown in Figure 1, the infrared markers were attached on the greater trochanter, medial and lateral femoral condyle and medial and lateral malleoli. In addition, two cluster markers were attached on the femur and on the leg. Primary position of the knee was 90-degree flexion; then, the subjects were requested to move their leg toward extension to test angle (20 or 60 degrees) with extension angle monitoring via motion analyzer cameras. We determined the joint angles to be tested according to previous studies (Baker et al, 2002; Bennell et al, 2005). Subjects were then asked to hold this position for 5 s. After that, they were instructed to return to the primary position. Following a 5-s rest period, they were requested to assume the previous angle and hold for 3 s. The difference between these two attempts was used to establish the target angle and defined as repositioning error before the treatment condition. The cameras of the motion analysis system (Qualysis, Gothenburg, Sweden) captured the test process. During testing, subjects wore a blindfold in order to eliminate visual cues. The test was repeated three times, and the average was considered for statistical analysis. The selection order of the test angles was random. This procedure was done before and immediately after the use of electrical stimulation applied via an electrical stimulator device (conventional TENS with the duration of 50 ms and 100 HZ frequency) through pairs of electrodes (Mascarin et al, 2012) placed on the medial and lateral joint line of the knee for 5 min. Finally, the absolute repositioning error before and after TENS application condition was measured.
Participants Thirty female subjects with minimal to moderate (Grades 1–3) medial compartment knee OA were recruited in the study. Women are more severely and more frequently affected by knee OA. Differences in knee anatomy, kinematics, previous knee injury and hormonal influences may play a role (Hame and Alexander, 2013). Therefore, we recruited just female subjects to eliminating intersubject differences. The grade of knee OA was assessed by using the modified Kellgren/Lawrence grading system. Subjects were included in the study if they had a diagnosis of medial compartment knee OA confirmed by a physician and if they demonstrated radiographic evidence of knee OA. All recruited subjects selected were referred to the physical therapy clinic of Shiraz Rehabilitation School. Subjects with severe KL grades were not recruited because it is unclear whether the stimulation applied would adequately penetrate the tissue around the knee and
Figure 1. V3D knee model.
Effects of TENS on joint position sense OA subjects
DOI: 10.3109/09593985.2014.903547
Initially, each subject’s threshold for detection of the stimulation was determined by applying the stimulation and incrementally increasing the amplitude until the subject indicated they detected the stimulation. The intensity was monitored throughout the period and turned up, if necessary, to maintain the specified level of the subject’s verbal report.
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Statistical analysis All statistical analyses were performed using SPSS 15 software (SPSS Inc., Chicago, IL). Normality distribution of the variables was checked by One-Sample Kolmogorov–Smirnov test. Descriptive statistics were calculated. To compare mean errors in joint re-positioning between angles (20 and 60 degrees) before and after electrical stimulation, paired t tests were employed. To compare the effect of electrical stimulation on JPS for both angles, independent sample t tests were performed for each angle tested. Pearson correlation was used to determine the relationship between the absolute error (degrees) of the subjects before TENS treatment and the improvement in absolute error seen in the condition for 60 degree angle repositioning.
Results Thirty subjects (40–60 years) with minimal to moderate medial knee OA were studied. The mean age and BMI of these participants were 51.1 (±7.45) years and 26.46 (±3.3), respectively (Table 1). Our population presented with Kellgren– Lawrence grades ranging from 1 to 3, were considered to be mild to moderately functionally impaired and were not excessively obese or elderly. The differences (mean errors) in the knee joint repositioning for both angles (20 and 60 degrees) were reduced significantly after applying sensory electrical stimulation (Table 2). The differences (mean errors) in 20 degrees, before application of sensory electrical stimulation, were significantly less than that in 60 degrees. However, after the application of sensory electrical stimulation, this difference in the mean error was not statistically significant (Table 2). Correlation analysis demonstrated a moderate to strong correlation between the absolute repositioning error before TENS treatment condition and the improvement seen in the absolute error with the TENS treatment condition for both angles of 20 degrees (R ¼ 0.646; p50.005) and angle of 60 degrees (R ¼ 0.555; p50.005; Figure 2).
Table 1. Mean (±SD) demographic information for all test subjects.
Age (years) Height (cm) Weight (kg) BMI (kg/m2) KL grade (1–3) Pain
Upper
Lower
Mean ± SD
60 165 80 33.6 1 6
40 141 55 21.0 3 3
51.1 ± 7.5 155.6 ± 6.3 63.8 ± 6.8 26.5 ± 3.3 2.1 ± 0.6 4.3 ± 0.9
Table 2. Differences (degrees) between the knee joint angle before and after application of sensory electrical stimulation. Before stimulation After stimulation In 20 degree position In 60 degree position
3.2 ± 5.2 4.4 ± 7.7 p ¼ 0.023
1.9 ± 2.4 3.0 ± 3.4 p ¼ 0.304
p ¼ 0.001 p ¼ 0.001
3
Discussion Our study was designed to examine whether TENS is effective on improving proprioception. Repositioning error was used as a criterion to for JPS and somewhat for proprioception (Newcomer et al, 2000). Proprioception can be measured in several different ways. In this study, we used JPS as a measure of proprioception. The results indicate that conventional TENS affects proprioception sense as measured by JPS. The results confirmed that repositioning error on a dynamic position sense task changes with TENS application. The findings of this study demonstrated that the mean of joint repositioning error in both 20 and 60 degrees reduced significantly after applying sensory electrical stimulation. The result of this study is comparable with that of Collins et al (2011). Collins et al (2011) also observed improvements in JPS followed by application of sensory electrical stimulation. In another study, Gravelle et al (2002) observed improvement in the sensitivity of the somatosensory system and balance in older people following electrical stimulation. They indicated improvement in balance because of improvement in proprioception. Gravelle et al (2002) ascribed this finding to small changes in receptor transmembrane potentials that were followed by application of electrical stimulation; this small change in the potential brings the neuron closer to the threshold and increases the possibility of action potential in response to weak signals. Birmingham et al (2001) also noted that the poorer the proprioceptive ability, the greater the improvement after application of an external stimulus. Since proprioception is mediated by afferent input from articular, muscular and cutaneous structures, the improvement in knee joint proprioception was likely due to increased afferent input. The afferent input was increased via enhancement of cutaneous stimulation, muscle spindle and Ruffini receptors, which are located in the ACL from an electrical stimulation; this explanation has also been proposed by others (Barrett, Cobb, and Bentley, 1991). The substantia gelatinosa (SG) cells in the dorsal horn receive afference from ‘‘pain’’ fibers (Ad-fibers and C-fibers), and is believed to modulate the synaptic transmission of nerve impulses from peripheral sensory and nociceptive fibers, to central cells. The gate control theory suggests that afference from large diameter sensory fibers facilitates the inhibitory cells of the SG that in turn block both sensory and nociceptive afference to the central transmission cells, which in turn relay to higher central nervous centers. The central transmission cell is inhibited, or in other words, the ‘‘gate’’ is closed causing not only subjective pain relief but also some reduction in sensory afference to higher centers. The effects of some rehabilitative therapies have been investigated on proprioception improvement including: massage therapy (Henriksen et al, 2004); muscle strengthening (Beard, Dodd, Trundle, and Simpson, 1994); and taping and bracing (Heit, Lephart, and Rozzi, 1996). Henriksen et al (2004) investigated the effects of stimulating massage on intra-individual error in relation to the repeating measurements of JPS, concluding that massage could be a treatment of choice in order to help subjects with reduced JPS following musculoskeletal or neurological pathologies. However, not all rehabilitation modalities studied so far have demonstrated positive effects on JPS. Callaghan, Selfe, Bagley, and Oldham (2002) investigated the effects of patellar taping on proprioception, finding that normal subjects with good proprioception did not benefit from patellar taping, and the authors justified that probably because the data from the good and poor groups canceled out (Callaghan, Selfe, Bagley, and Oldham, 2002). Lund et al (2009) found that massage had no effect on the immediate joint repositioning error in subjects with knee OA, and they concluded that maybe joint
4
Z. R. Shirazi et al.
Physiother Theory Pract, Early Online: 1–5
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
Figure 2. The relationship between the absolute error (degrees) of the subjects before TENS treatment and the improvement in absolute error seen in the condition for 60 degree angle repositioning.
repositioning error is not sufficiently sensitive to identify possible effects of massage on proprioception. Moreover, the results of this study showed that before application of TENS, the error size in 60 degrees was significantly less than that in 20 degrees. After applying TENS, the mean errors reduced between two angle positions, but this difference was not significant. This can indicate that TENS could affect proprioceptive receptors in both positions and increase their sensitivity. Our findings also suggest that the transcutaneous electrical stimulation may be most beneficial to apply in subjects with larger proprioceptive deficits. The sensory electrical stimulation used in this study is probably effective in enhancing the function of the human sensorimotor system because of the electrical nature of information transfer in the sensory neurons (Collins et al, 2011). A somatosensory feedback is an essential part of the proprioceptive system (Collins et al, 2011). Therefore, improvement in this sense following the use of TENS increases the sensory afferents. While this study is novel, it has several limitations such as lack of control group and lack of investigation of other sensory amplitude levels.
Conclusion The aim of our study was to determine if TENS might improve JPS. There was significant difference in the JPS before and after TENS treatment. Conventional TENS with sensory threshold amplitude seems to have positive impact on proprioception sense in the knee joint as measured by JPS in subjects with knee OA. Our findings suggest that TENS may be most beneficial to apply in subjects with larger proprioceptive deficits. Future work is necessary to determine if applying different types of TENS with different amplitudes will improve knee proprioception. Further investigations in larger populations and with a well-defined RCT design are needed in subjects with known proprioceptive deficiencies.
Acknowledgements We would like to thank the subjects who participated in the study and also Dr. Nasrin Shokrpour at the Center for Development of Clinical Research of Nemazee Hospital for editorial assistance. This study is extracted from the proposal number 5683 and R. Shafaei’s MSc Thesis.
Declaration of interest The authors report no declarations of interest. This work was financially supported by Shiraz University of Medical Sciences.
References Baker V, Bennell K, Stillman B, Cowan S, Crossley K 2002 Abnormal knee joint position sense in individuals with patellofemoral pain syndrome. Journal of Orthopaedic Research 20: 208–214. Baliunas A, Hurwitz D, Ryals A, Karrar A, Case J, Block J, Andriacchi T 2002 Increased knee joint loads during walking are present in subjects with knee osteoarthritis. Osteoarthritis and Cartilage 10: 573–579. Barrett DS, Cobb AG, Bentley G 1991 Joint proprioception in normal, osteoarthritic and replaced knees. Journal of Bone and Joint Surgery (Br) 73: 53–56. Beard DJ, Dodd CA, Trundle HR, Simpson AH 1994 Proprioception enhancement for anterior cruciate ligament deficiency. A prospective randomised trial of two physiotherapy regimes. Journal of Bone and Joint Surgery (Br) 76: 654–659. Bennell KL, Wee E, Crossley K, Stillman B, Hodges P 2005 Effects of experimentally-induced anterior knee pain on knee joint position sense in healthy individuals. Journal of Orthopaedic Research 23: 46–53. Bennell KL, Hinman RS, Metcalf BR, Crossley KM, Buchbinder R, Smith M, McColl G 2003 Relationship of knee joint proprioception to pain and disability in individuals with knee osteoarthritis. Journal of Orthopaedic Research 21: 792–797. Birmingham T, Kramer J, Kirkley A, Inglis J, Spaulding S, Vandervoort A 2001 Knee bracing for medial compartment osteoarthritis: Effects on proprioception and postural control. Rheumatology 40: 285–289.
Physiother Theory Pract Downloaded from informahealthcare.com by University of Southern California on 04/07/14 For personal use only.
DOI: 10.3109/09593985.2014.903547
Bopf D, McAuliffe M, Shillington M, Drynan D, Bucknell E 2010 Knee osteoarthritis: Use of investigations and non-operative management in the Australian primary care setting. Australasian Medical Journal 1: 194–197. Callaghan MJ, Selfe J, Bagley PJ, Oldham JA 2002 The effects of patellar taping on knee joint proprioception. Journal of Athletic Training 37: 19–24. Collins AT, Blackburn JT, Olcott CW, Miles J, Jordan J, Dirschl DR, Weinhold PS 2011 Stochastic resonance electrical stimulation to improve proprioception in knee osteoarthritis. Knee 18: 317–322. Collins JJ, Imhoff TT, Grigg P 1996 Noise-enhanced tactile sensation. Nature 383: 770. Cordo P, Inglis JT, Verschueren S, Collins JJ, Merfeld DM, Rosenblum S, Buckley S, Moss F 1996 Noise in human muscle spindles. Nature 383: 769–770. Devanne H, Maton B 1998 Role of proprioceptive information in the temporal coordination between joints. Experimental Brain Research 119: 58–64. Dhruv NT, Niemi JB, Harry JD, Lipsitz LA, Collins JJ 2002 Enhancing tactile sensation in older adults with electrical noise stimulation. Neuroreport 13: 597–600. Dickstein R, Laufer Y, Katz M 2006 TENS to the posterior aspect of the legs decreases postural sway during stance. Neuroscience Letters 393: 51–55. Felson DT, Zhang Y 1998 An update on the epidemiology of knee and hip osteoarthritis with a view to prevention. Arthritis and Rheumatism 41: 1343–1355. Gravelle DC, Laughton CA, Dhruv NT, Katdare KD, Niemi JB, Lipsitz LA, Collins JJ 2002 Noise-enhanced balance control in older adults. Neuroreport 13: 1853–1856. Grob K, Kuster M, Higgins S, Lloyd D, Yata H 2002 Lack of correlation between different measurements of proprioception in the knee. Journal of Bone and Joint Surgery (Br) 84: 614–618. Hame SL, Alexander RA 2013 Knee osteoarthritis in women. Current Reviews in Musculoskeletal Medicine 6: 182–187. Hartrick CT, Kovan JP, Shapiro S 2003 The numeric rating scale for clinical pain measurement: A ratio measure? Pain Practice 3: 310–316. Heiden TL, Lloyd DG, Ackland TR 2009 Knee joint kinematics, kinetics and muscle co-contraction in knee osteoarthritis patient gait. Clinical Biomechanics 24: 833–841. Heit EJ, Lephart SM, Rozzi SL 1996 The effect of ankle bracing and taping on joint position sense in the stable ankle. Journal of Sport Rehabilitation 5: 206–213. Henriksen M, Højrup A, Lund H, Christensen L, Danneskiold-Samsøe B, Bliddal H 2004 The effect of stimulating massage of thigh muscles on knee joint position sense. Advances in Physiotherapy 6: 29–36. Hijmans JM, Geertzen JHB, Zijlstra W, Hof AL, Postema K 2008 Effects of vibrating insoles on standing balance in diabetic neuropathy. Journal of Rehabilitative Research and Development 45: 1441–1450. Hortoba´gyi T, Westerkamp L, Beam S, Moody J, Garry J, Holbert D, DeVita P 2005 Altered hamstring-quadriceps muscle balance in subjects with knee osteoarthritis. Clinical Biomechanics 20: 97–104. Hurley MV, Scott DL, Rees J, Newham DJ 1997 Sensorimotor changes and functional performance in subjects with knee osteoarthritis. Annals of the Rheumatic Diseases 56: 641–648. Itoh K, Hirota S, Katsumi Y, Ochi H, Kitakoji H 2008 A pilot study on using acupuncture and transcutaneous electrical nerve stimulation
Effects of TENS on joint position sense OA subjects
5
(TENS) to treat knee osteoarthritis (OA). Chinese Medicine 3: 2. doi: 10.1186/1749-8546-3-2. Kirkley A, Webster-Bogaert S, Litchfield R, Amendola A, MacDonald S, McCalden R, Fowler P 1999 The effect of bracing on varus gonarthrosis. Journal of Bone and Joint Surgery (Am) 81: 539–548. Knoop J, Steultjens M, van der Leeden M, van der Esch M, Thorstensson C, Roorda L, Lems W, Dekker J 2011 Proprioception in knee osteoarthritis: A narrative review. Osteoarthritis and Cartilage 19: 381–388. Lephart SM, Pincivero D, Giraido J, Fu FH 1997 The role of proprioception in the management and rehabilitation of athletic injuries. American Journal of Sports Medicine 25: 130–137. Lund H, Henriksen M, Bartels EM, Danneskiold-Samsøe B, Bliddal H 2009 Can stimulating massage improve joint repositioning error in subjects with knee osteoarthritis? Journal of Geriatric Physical Therapy 32: 111–116. Lund H, Juul-Kristensen B, Hansen K, Christensen R, Christensen H, Danneskiold-Samsøe B, Bliddal H 2008 Movement detection impaired in subjects with knee osteoarthritis compared to healthy controls: A cross-sectional case-control study. Journal of Musculoskeletal and Neuronal Interactions 8: 391–400. Mascarin N, Vancini R, dos Andrade M, de Magalha˜es E, de Lira CA, Coimbra I 2012 Effects of kinesiotherapy, ultrasound and electrotherapy in management of bilateral knee osteoarthritis: Prospective clinical trial. BMC Musculoskeletal Disorders 13: 182–190. Mima T, Oga T, Rothwell J, Satow T, Yamamoto J-i, Toma K, Fukuyama H, Shibasaki H, Nagamine T 2004 Short-term high-frequency transcutaneous electrical nerve stimulation decreases human motor cortex excitability. Neuroscience Letters 355: 85–88. Newcomer KL, Laskowski ER, Yu B, Johnson JC, An KN 2000 Differences in repositioning error among subjects with low back pain compared with control subjects. Spine 25: 2488–2493. Osiri M, Welch V, Brosseau L, Shea B, McGowan J, Tugwell P, Wells G 2009 Transcutaneous electrical nerve stimulation for knee osteoarthritis. Cochrane Database of Systematic Reviews 4: CD002823. Pai YC, Rymer WZ, Chang RW, Sharma L 1997 Effect of age and osteoarthritis on knee proprioception. Arthritis and Rheumatism 40: 2260–2265. Priplata A, Niemi J, Salen M, Harry J, Lipsitz LA, Collins J 2002 Noiseenhanced human balance control. Physical Review Letters 89: 238101– 238104. Priplata AA, Patritti BL, Niemi JB, Hughes R, Gravelle DC, Lipsitz LA, Veves A, Stein J, Bonato P, Collins JJ 2006 Noise-enhanced balance control in subjects with diabetes and subjects with stroke. Annals of Neurology 59: 4–12. Sharma L 1999 Proprioceptive impairment in knee osteoarthritis. Rheumatic Diseases Clinics of North America 25: 299–314. Sharma L, Pai YC, Holtkamp K, Rymer WZ 1997 Is knee joint proprioception worse in the arthritic knee versus the unaffected knee in unilateral knee osteoarthritis? Arthritis and Rheumatism 40: 1518–1525. Sluka KA, Walsh D 2003 Transcutaneous electrical nerve stimulation: Basic science mechanisms and clinical effectiveness. Journal of Pain 4: 109–121. Solomonow M, D’Ambrosia R 1991 Neural reflex arcs and muscle control of knee stability and motion. In: Scott WN (ed) Ligament and extensor mechanism injuries of the knee, pp 389–400. St. Louis, Mosby Year Book.
