Neuromuscular Electrical Stimulation (NMES) Reduces Structural and Functional Losses of Quadriceps Muscle and Improves Health Status in Patients with Knee Osteoarthritis Marco Aure´lio Vaz,1 Bruno Manfredini Baroni,1 Jeam Marcel Geremia,1 Fa´bio Juner Lanferdini,1 Alexandre Mayer,1 Adamantios Arampatzis,2 Walter Herzog3 1
Exercise Research Laboratory, School of Physical Education, Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil, Centre of Sport Science and Sport Medicine, Department of Training and Movement Sciences, Humboldt-Universita¨t zu Berlin, Berlin, Germany, 3 Faculty of Kinesiology, Human Performance Laboratory, University of Calgary, Calgary, Alberta, Canada 2
Received 17 January 2012; accepted 11 October 2012 Published online 8 November 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22264
ABSTRACT: Knee osteoarthritis (OA) is associated with quadriceps atrophy and weakness, so muscle strengthening is an important point in the rehabilitation process. Since pain and joint stiffness make it often difficult to use conventional strength exercises, neuromuscular electrical stimulation (NMES) may be an alternative approach for these patients. This study was aimed at (1) identifying the associations of knee OA with quadriceps muscle architecture and strength, and (2) quantifying the effects of a NMES training program on these parameters. In phase 1, 20 women with knee OA were compared with 10 healthy female, asymptomatic, age-matched control subjects. In phase 2, 12 OA patients performed an 8-week NMES strength training program. OA patients presented smaller vastus lateralis thickness (11.9 mm) and fascicle length (20.5%) than healthy subjects (14.1 mm; 24.5%), and also had a 23% smaller knee extensor torque compared to the control group. NMES training increased vastus lateralis thickness (from 12.6 to 14.2 mm) and fascicle length (from 19.6% to 24.6%). Additionally, NMES training increased the knee extensor torque by 8% and reduced joint pain, stiffness, and functional limitation. In conclusion, OA patients have decreased strength, muscle thickness, and fascicle length in the knee extensor musculature compared to control subjects. NMES training appears to offset the changes in quadriceps structure and function, as well as improve the health status in patients with knee OA. ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 31:511–516, 2013 Keywords: osteoarthritis; muscle architecture; muscle strength; WOMAC; electrical stimulation
Osteoarthritis (OA) is one of the major degenerative diseases and it affects elderly women more frequently than elderly men.1,2 The prevalence of OA is expected to increase dramatically in the near future due to the increased life expectancy and an increasing rate of obesity of the world population.3 The knee is the most affected joint with 13.6% of women above 60 years showing radiographic evidence of OA and/or clinical symptoms.2 OA causes erosion of articular cartilage, weakening of subchondral bone, meniscal degeneration, inflammation of the synovium, and intra-articular osteophytes.4 These changes lead to a reduction in the range of motion, and increase in joint stiffness and pain.5 In addition to the effects on the joint structure and function, OA also has a negative effect on the musculoskeletal system. Patients with knee OA have decreased knee extensor strength compared to healthy subjects6–10 and compared to the healthy contralateral limb.11,12 Evidence also suggests that the muscle weakness is associated with a decrease in muscle mass.11,12 However, although a reduction in muscle thickness11 and anatomical cross-sectional area12 have been described in OA patients, we were unable to find evidence on how muscle weakness was related to changes in other muscle architecture parameters associated with strength, such as fascicle length, and pennation angle.
Correspondence to: Marco Aure´lio Vaz (T: þ5551-33085860; F: þ5551-33085858; E-mail:
[email protected]) ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
Fascicle length is related to the number of sarcomeres aligned in series in the muscle cells, which affects the maximal contracting velocity and the optimal length for force generation.13 Pennation angle has been associated with the amount of in parallel sarcomeres, which is closely related to the maximal force capacity of a muscle fiber.13 Therefore, determining the above parameters allow for a better understanding on how these intrinsic changes in muscle architecture affect functionality in OA patients. Knee extensor strength is a predictor of independence in the elderly and an indicator for life span.14 Patients with knee OA often have significant functional limitations,6 leading to a vicious cicle of pain–weakness–pain. In addition, quadriceps weakness has been related to decreases in proprioception,15 joint stabilization,16 and shock absorption,17 contributing to a progression of joint degeneration with a subsequent increase in joint pain.12,18 Epidemiological studies have concluded that quadriceps muscle weakness may lead to incident symptomatic knee OA, although the results were not statistically significant and contained body mass as a confounding factor.19 Moreover, studies in animal model demonstrated that muscle weakness causes increased joint degeneration,20 providing evidence that muscle weakness might be a risk factor for the onset and progression of OA.21 Scientific evidence emphasizes the possible importance of quadriceps strengthening in the prevention and rehabilitation of knee OA.3,18,21 However, pain and joint stiffness make it often difficult to use JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013
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conventional strength training programs. Neuromuscular electrical stimulation (NMES) may be an alternative, low cost, efficient, and less painful approach than voluntary knee extensor exercises for patients with knee OA. NMES is considered an efficient technique for quadriceps strengthening22 and has been used to treat patients with knee OA. Although previous studies found increases in health and knee function after NMES training,23–28 the muscular adaptations of NMES in patients with knee OA have not been described. The present study had the following goals: (1) to identify the associations of knee OA with structural (muscle architecture) and functional (knee extensor torque) parameters of the knee extensor muscles in elderly women; and (2) to quantify the possible effects of an 8-week NMES strength training program on these structural and functional parameters in this patient population.
METHODS Experimental Design This study was approved by the University’s Research Ethics Committe (Protocol #2007791) and all subjects signed an informed consent form prior to participation. The study was comprised of two parts. In phase 1, we quantified the effects of knee OA on the structural and functional properties of the knee extensor muscles, and in phase 2 we characterized the effects of a NMES strength training program on these properties. Subjects Patients with knee OA were recruited from a hospital and two orthopaedic clinics. Subjects were chosen based on the following inclusion criteria: (1) women, minimum age of 50 years; (2) clinically diagnosed with knee OA; (3) no contraindications to execute maximal knee extension tests (e.g., cardiorespiratory complications); (4) no previous musculoskeletal or joint injuries besides knee OA; (5) no hip or knee surgery; and (6) no neurological problems. All patients received an intial clinical assessment, including knee X-rays to support the clinical diagnosis of OA. Xrays included an axial patellar view obtained at 308 of knee flexion (08 ¼ full extension), an antero-posterior monopodal weightbearing (long view), a sagittal monopodal (long view); and an antero-posterior Schuss incidence with 308 of knee flexion (long view). X-ray images were used to determine the degree of OA, according to the criteria proposed by Dejour et al.29 Only patients diagnosed with a degree 2 or 3 of knee OA were included in the study. In phase 1 of this study, the structural and functional properties of the quadriceps muscles of 20 women with knee OA and 10 healthy female, asymptomatic, age-matched control subjects were assessed. The characteristics of the patient and control groups subjects are presented in Table 1. In phase 2, 12 of the 20 OA patients volunteered to participate in the 8-week NMES strength training program (age ¼ 58 8 years; height ¼ 1.55 0.08 m; body mass ¼ 78 15 kg; body mass index ¼ 32 7 kg/m2). These OA patients were submitted to clinical evaluation and assessment of the structural and functional properties of the quadriceps muscles before and after the NMES strength training program. JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013
Table 1. Characteristics of the OA Patients Group and Healthy Controls Group (Mean SD) Healthy Subjects (n ¼ 10) Age (years) Height (cm) Body mass (kg) Body Mass Index (kg/m2)
60 157 66 27
7 1 7 3
OA Patients (n ¼ 20) 61 156 72 30
8 7 11 5
p-value 0.797 0.116 0.605 0.065
Testing Procedures Muscle Architecture An ultrassound system (SSD 4000, 51 Hz, ALOKA Inc., Japan) with a linear array probe (60 mm, 7.5 MHz), was used to determine the thickness, fascicle length, and pennation angle of the vastus lateralis muscle. Ultrassound images were obtained at rest with the subject sitting on the chair of an isokinetic dynamometer (Biodex System 3; Biodex Medical Systems, Shirley, NY) with the hip and knee flexed at 858 and 908, respectively. All images were captured in the sagittal plane of vastus lateralis (at midway between the lateral condyle of the femur and the greater trochanter).30 The ultrasound probe was positioned in the approximate direction of the vastus lateralis muscle fibers (long axis with respect to the limb).30 The same experienced researcher made all evaluations and this researcher was blinded to the study group. Ultrasound images were analyzed off-line using ImageJ software (National Institute of Health, Bethesda, MD). Muscle thickness was defined as the distance between the deep and the superficial aponeuroses. The pennation angle was defined as the angle between the deep aponeurosis and the fascicle orientation. Fascicle length was defined as the length of the fascicular trajectory between the fascicle insertions on the superficial and deep aponeuroses. Since this length usually was greater than the probe surface, the fascicle line was extrapolated and calculated through a mathematical routine in MATLAB (MathWorks, Natick, MA). Fascicle lengths were normalized to femur length (obtained from the X-ray images) and are reported as percentage values. In a pilot study to test the intra-rater reliability of our measurements, we found ICC values of 0.91 for muscle thickness, 0.91 for pennation angle, and 0.90 for fascicle length. Knee Extensor Torque Maximal isometric knee extensor torques were obtained on an isokinetic dynamometer (Biodex System 3; Biodex Medical Systems). Participants were positioned on the dynamometer according to the manufacturer’s recommendations. After a warm-up and a familiarization session, each subject executed three maximal isometric knee extensor contractions with the knee fixed at a flexion angle of 608. Each contraction lasted for 5 s and a 2-min interval was observed between consecutive contractions. Peak torque values from each contraction were obtained and an additional contraction was obtained if a torque variation higher than 10% was observed between consecutive contractions. The highest value from the three maximal isometric contractions was used for data analysis. Clinical Evaluation The Western Ontario and McMaster Universities Arthritis Index (WOMAC), including all three subscales (measured by
NMES TRAINING FOR KNEE OSTEOARTHRITIS
a Likert version and the possible range of scores is 0 ¼ none to 4 ¼ extreme)25 were used to determine the degree of functionality of the OA patients before and after NMES strength training program. Strength Training NMES Program A portable stimulator, designed for this study, was used for the strength training NMES program. The intervention was performed with subjects seated on a regular chair (hip and knee angles maintained at approximately 908), 3 times/week for a period of 8 weeks. Patients performed the 24 strength training sessions under the supervision of a member of the research team. This researcher was responsible for the adequate positioning of the surface stimulation electrodes (5 cm 13 cm; Axelgaard Mfg. Co., Ltd., Fallbrook, CA) and for the control of the electrical stimulation intensity, which was set at the maximum that could be comfortably tolerated by the patients. Subjects were instructed to relax and avoid voluntary contractions of the knee extensors during the training sessions. NMES parameters included: rectangular biphasic symmetric current, pulse duration of 400 ms and stimulation frequency of 80 Hz. The first training session lasted 18 min and was comprised of 10 s of stimulation followed by 50 s of rest. Training progression was achieved by a gradual increase in the total session time and a reduction of the resting period, resulting in an increased number of contractions per time interval, and, therefore, greater exposure time of the knee extensor muscles to NMES (Table 2). Statistical Analysis Independent Student’s t-tests were used to quantify possible differences in muscle thickness, fascicle length, angles of pennation, and knee extensor torques between OA patients and the healthy control group in part 1 of the study. Student’s paired t-tests were used for the within group comparisons between pre- and post-NMES intervention. A 5% (p < 0.05) significance value was adopted for all tests (SPSS for Windows, 17.0 version, USA). All values are presented as means and 1 standard deviation in the text and means and 1 standard error in the figures.
RESULTS OA patients and healthy subjects presented similar femur lengths (446 16 mm and 444 19 mm, respectively). Vastus lateralis thickness and fascicle length were smaller in OA patients (11.9 2.5 mm; 20.5 6.0%) compared to healthy subjects Table 2. NMES Strength Training Program Week 1 2 3 4 5 6 7 8
Total Time (min)
Contraction–Rest (s)
Contraction Time (s)
18 20 22 24 26 28 30 32
10–50 10–50 10–40 10–40 10–30 10–30 10–20 10–20
180 200 264 288 390 420 600 640
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(14.1 2.5 mm; 24.5 4.6%), while pennation angles were the same for the OA and control subject groups. Subjects in the OA group also had a 23% smaller knee extensor torque compared to the healthy control subjects (Fig. 1). NMES training increased vastus lateralis thickness (from 12.6 1.3 to 14.2 2.1 mm) and fascicle length (from 19.6 4.6% to 24.6 4.4%) from pre- to posttraining, but had no significant effect on the pennation angle. Additionally, NMES training increased the maximal isometric knee extensor torque by 8% (Fig. 2). OA patients showed improvements in WOMAC scores following the NMES training program (Table 3). The intervention program promoted a reduction of 38% in joint pain, 29% in joint stiffness, and 34% in functional limitation.
DISCUSSION The primary results of this study are (1) that women with knee OA are weaker, have smaller muscles and shorter fascicle length in VL compared to age- and sex-matched normal control subjects; (2) that NMES strength training program in women aged 47–75 years with knee OA increases strength, muscle thickness, and fibre lengths in VL; and (3) that these muscular changes following NMES training are associated with improvements in clinical outcome scores. Loss in quadriceps muscle mass in OA patients has been associated with decreases in muscle thickness11 and cross-sectional area,12 and our results are in agreement with these previous findings. However, Mairet et al.11 did not find decreases in fascicle lengths, as we found here. Muscle atrophy is sometimes associated with a decrease in the pennation angle of muscles.13 However, we found no changes in the angles of pennation, neither between the normal and OA patient group nor following the NMES training intervention, possibly because of an accumulation of intramuscular fat and connective tissue sometimes found in atrophied muscles of OA patients.11,12 However, our results do not allow for evaluation of this hypothesis, as fat content and possible fibrosis were not evaluated in our patient group. The smaller muscle thickness in the OA patients compared to the control group subjects can be directly explained with the smaller fascicle length as the pennation angle was the same in OA patients and control subjects. A muscle with shorter fascicle length will show a smaller capacity of force production at longer lengths.13 As most studies comparing OA patients with asymptomatic subjects6,7,9,10 evaluated the knee extensor muscles with tests performed with the knee at 908 of flexion (descending limb of the torqueangle quadriceps relationship), the quadriceps muscle of the OA patients was more distant from its optimal length (or joint angle) for force production, which may have contributed for the reduced levels of force produced at this specific joint angle. JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013
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Figure 1. Knee extensor torque and vastus lateralis muscle architecture from healthy and osteoarthritis patient groups (mean SE). p < 0.05.
The NMES strength training program was successful in counteracting the deleterious effects of OA on the knee extensor muscles. NMES reduced muscle weakness and increased muscle thickness and fascicle length. The post-NMES training values of the OA patients were close to the values of the healthy control group, suggesting that artificial electrical stimulation
offsets most of the OA-induced structural and functional losses of the knee extensor muscles. Our results for isometric knee extensor torque gains are similar to the results reported by Talbot et al.23 following 12 weeks, 3 times/week, of NMES training in OA patients. Durmus et al.26 found increments of about 35% in the one maximal repetition test after 5
Figure 2. Knee extensor torque and vastus lateralis muscle architecture from OA patients before and after NMES strength training (mean SE). p < 0.05. JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013
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Table 3. WOMAC Scores from OA Patients before and after the 8-Week NMES Strength Training Program (Mean SD) WOMAC Domain Joint pain Joint stiffness Functional limitation
Baseline
Post-Training
p-value
11.7 3.2 5.1 1.6 44.9 7.8
7.2 3.5 3.6 1.7 29.7 12.8
0.005 0.075 0.001
weekly sessions of NMES training during 4 weeks, while Rosemffet et al.25 did not observe any significant gain in isometric force after 8 weeks of training with three NMES sessions per week. These different outcomes with apparently similar NMES stimulation training protocols might be associated with the methods for evaluating maximal strength, to the level of impairment of the OA patients, or the detailed parameters chosen for the NMES training programs (current, duration, frequency, etc.). Since some NMES interventions produce significant improvements in knee extensor strength and muscle maintenance, it seems important that NMES protocols are optimized for each patient. A reduced capacity for activating the knee extensor muscles (muscle inhibition) is a well documented adjunct of knee OA.6–12 The mechanisms of this inhibition are unknown and need to be determined for effective restoration of voluntary force and control of the knee extensors. Improvements in voluntary activation of the quadriceps muscles after a period of a NMES training program have been demonstrated in young healthy subjects.31,32 Therefore, although the mechanisms on how NMES reduces muscle inhibition are not clear in the literature,33 the strength gains observed in our study after NMES training may partly be associated with an improvement in activation capacity of the quadriceps muscle. This possibility should be addressed in future investigations. There is strong evidence in the literature that strength exercise has positive effects on pain scores and functional outcomes in knee OA patients.34 Specifically, OA patients have shown a significant decrease in pain,23–28 a reduction in joint stiffness,26,27 an increase in joint range of motion,28 and an improvement in functional performance23,26 following NMES training. Although we cannot establish a direct causative association between muscle strength and health status, stronger knee extensor muscles are thought to decrease impact forces at the knee joint,16,17 and might reduce the mechanical stimuli for pain,18 thereby relieving the pain symptoms of the patients. Our findings of improved WOMAC scores suggest that NMES should be considered as a treatment option for the prevention of ‘‘at risk’’ populations and/or the treatment of patients with early OA in the knee. Nevertheless, our results for the WOMAC scores might have been biased due to the fact that all patients already knew
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that they were in a treatment group, and is a limitation of our study. In conclusion, patients with knee OA have decreased strength, muscle thickness, and fascicle length in the knee extensor musculature compared to ageand sex-matched controls. NMES training of short duration appears to offset the changes in quadriceps structure and function, as well as reduces joint pain, joint stiffness, and functional limitation in patients with knee OA.
ACKNOWLEDGMENTS The authors would like to acknowledge FINEP-Brazil, CNPq-Brazil, and CAPES-Brazil for financial support. The authors would also like to thank Cintia Helena Ritzel, Silvia ˆ ngela Muraro, Rafael Fortuna, and Profs. Helena Manfrin, A ˜ Fernando Aragao and Rafael Baptista for technical help in different phases of the study, and Danton Pereira da Silva Junior and Joel Machado dos Santos for the development of the portable stimulator.
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