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DOI: 10.1055/s-0039-1688551
Changes in Maximal Isometric Quadriceps Strength after the Application of Ultrasound-Guided Percutaneous Neuromodulation of the Femoral Nerve: A Case Series
Article in several languages: English | españolAddress for correspondence
Publication History
Publication Date:
28 June 2019 (online)
- Abstract
- Introduction
- Materials and Methods
- Statistical Analysis
- Results
- Discussion
- Conclusions
- References
Abstract
Introduction For those individuals who have suffered an injury to the knee or undergone a surgical intervention, the early recovery of the muscle strength contraction properties of the quadriceps is essential for a favorable recovery and for a return to the activities of daily living and other work- or sports-related activities.
Objectives To evaluate the changes in maximal isometric strength (MIS) of the quadriceps muscle after the application of ultrasound-guided percutaneous neuromodulation (US-guided PNM) on the femoral nerve.
Materials and Methods A case series involving subjects who had previously presented unilateral knee pathology and were in the stage of recovery of quadriceps strength. The subjects were pain-free at the time of the dynamometry measurements, which were performed before and after the application of the US-guided PNM technique. The isometric measurement was performed using the KINEO dynamometry system, performing a preintervention measurement of the mean maximal isometric strength (mMIS) based on 3 repetitions (3 seconds contraction and 6 seconds relaxation). The US-guided PNM technique was performed on the femoral nerve, using the Physio Invasiva CE0120 device (Prim Physio, Madrid, Spain) and a GE Logiq e R7 ultrasound (GE Healthcare, Chicago, IL, USA).
Results In total, 13 subjects participated in the present study. Significant changes were obtained (p < 0.001) in the mMIS of the quadriceps of the affected knee, which progressed from a mean strength of 25.91 kg (standard deviation [SD]: 7.17 kg) to a mean strength of 29.98 kg (SD: 9.06 kg).
Discussion In subjects with knee pathology, the quadriceps muscle is inhibited despite being pain-free during the strength measurements. This process of inhibition can improve with the application of low frequency percutaneous electrical stimulation on the femoral nerve. This technique represents a complementary strategy for the recovery of the normal strength values in pathological knees with or without prior surgery.
Conclusions Ultrasound-guided PNM is an effective technique for the reestablishment of quadriceps strength in inhibited muscles.
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Keywords
ultrasound-guided percutaneous neuromodulation - invasive physical therapy - dynamometer - femoral nerve - isometric contractionIntroduction
Weakness of the quadriceps muscle after either an injury to the knee or knee surgery is a common impairment described in the literature.[1] [2] [3] This weakness is defined as muscle inhibition of articular origin.[4] [5] [6] The early restoration of the muscle contraction properties of the quadriceps is essential to ensure appropriate recovery and facilitate the return to the activities of daily living, as well as to work and/or sports activities.[7] [8] [9]
Among the various types of muscle contraction, maximal isometric strength (MIS, or maximal isometric voluntary contraction [MIVC]), is an essential parameter of strength for the correct functioning of the muscle motor unit.[10] [11] [12] Conditioned muscle inhibition can effectively decrease this variable.
Furthermore, a correlation exists between MIS and maximal concentric and eccentric strength.[13] [14] Several studies have found that MIS is vital during the performance of functional activities, such as jumping, cycling or running.[15] [16] Therefore, MIS is an essential variable in neuromuscular assessments.
The electrical stimulation of the peripheral nervous system is a therapeutic strategy that has been primarily used for the treatment of chronic pain for the past 50 years.[17] [18] This stimulation produces a modification of the input to the central nervous system, known as neuromodulation[19] [20] [21] [22] .
Currently, various neuromodulation procedures have been described in the health sciences,[23] such as brain stimulation, spinal cord stimulation, and peripheral stimulation. Ultrasound-guided percutaneous neuromodulation (US-guided PNM) is a recently developed invasive physical therapy technique used for neurofunctional improvement and for the treatment of pain.[23] To date, no studies have related this technique with muscle stimulation and dynamometry changes. Dynamometric tests with devices that enable the calculation of variables related with isometric movement are another form of functional assessment tools.[24] [25]
The aim of the present study was to evaluate changes in isometric strength measured using dynamometry, after the application of US-guided PNM in the femoral nerve.
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Materials and Methods
Design
A quasi-experimental study with a single intervention group, in which the mean maximal isometric strength (mMIS) was measured, using dynamometry, before and after an intervention with PNM at the level of the femoral nerve of both quadriceps muscles.
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Sample
The study subjects were voluntary participants > 18 years old recruited among patients of the Fisiocéano clinic (Móstoles, Madrid, Spain). The inclusion criteria were: subjects with previous pathology in one of their knees but without pain at the time of study, with variation coefficients[26] < 15% and who were in the stage of quadriceps muscle recovery. Subjects with pathologies that caused pain during the measurements and for whom dynamometry was contraindicated were excluded (acute muscle injuries, important joint instability, or acute joint inflammation, among others). For the use of US-guided PNM, the main contraindications were needle phobia, epilepsy, pacemaker, and pregnancy. All of the subjects signed the corresponding informed consent form to participate in the study.
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Measurements Performed
An expert on dynamometry, external to the physiotherapist who performed the intervention, performed the measurements and collected the strength data for statistical analysis. An isometric measurement of the quadriceps muscle was performed using the KINEO (GLOBUS, Codognè, Italia) dynamometry system. The assessment protocol consisted of a preintervention measurement of the mMIS (3 seconds contraction and 6 seconds relaxation, for a total of 3 repetitions) of both quadriceps muscles, and a postintervention measurement of the mMIS of the quadriceps on the side of the pathological knee. The assessment position was 90° of hip flexion and 45° of knee flexion, without straps and with manual grips on lateral supports. The lever arm was placed 2 cm from the malleolus on the ventral aspect of the ankle, without straps.[10]
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Physiotherapy Interventions
The US-guided PNM intervention consisted specifically of the application of a biphasic asymmetric electrical current compensated with a rectangular positive phase and a negative triangular phase, with a frequency of 10 Hz, a pulse width of 240 μs, and maximal tolerated intensity. This was in order to provoke a pain-free maximal muscle contraction, according to the following protocol: 10 stimulations with a duration of 10 seconds, with a 10-second rest period between each stimulation, as proposed by Minaya et al.[23] The certified device employed for the percutaneous application of the electrical current was the Physio Invasiva® CE0120 (Prim Fisioterapia y Rehabilitación, Madrid, Spain) using the PES modality, with 0.30 mm × 40 mm Physio Invasiva® needles (Prim Fisioterapia y Rehabilitación, Madrid, Spain). The femoral nerve was located over the femoral triangle, using the GE Logic R7 US machine (GE Healthcare, Chicago, IL, USA) with a 12L linear probe, in a transverse section. The needle was inserted using an inplane approach, with an angle of 45° to the skin surface, until reaching the epineurium of the femoral nerve at its lower and lateral aspect ([Fig. 1]). The axonal topography described for this nerve[27] shows how, at this site, the greater part of the motor axons of the quadriceps muscle are located ([Fig. 2]). Prior to the insertion of the needle, the skin was cleaned using isopropyl alcohol and chlorhexidine (Lainco® 2% antiseptic for clean skin). The intervention was performed by a physiotherapist with > 10 years of experience in invasive procedures and US assessments.




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Statistical Analysis
A descriptive analysis was performed by calculating the mean, the median and the mode of the characteristics of the dependent and independent variables. Inferential statistics were performed via the comparison of the means using the Student-t test (α= 0.05) for related samples, after considering the normality of the sample and the distribution of the kinetic samples assessed by dynamometry or via biomechanical systems. All of the analyses were performed using the Microsoft Excel 2013 software (Microsoft Corporation, Redmond, WA, USA).
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Results
In total, 13 voluntary subjects participated in the present study, with a mean age of 39.92 years old (standard deviation [SD]: 9.09), of which 2 were female and 11 were male. [Table 1] presents the sociodemographic and clinical characteristics of the sample.
Subject |
Gender |
Age |
Height (cm) |
Weight (Kg) |
Pathological side |
Type of lesion |
---|---|---|---|---|---|---|
01 |
F |
44 |
166 |
52 |
L |
Condropathy |
02 |
F |
28 |
162 |
64 |
L |
Rupture anterior cruciate ligament |
03 |
M |
38 |
188 |
78 |
R |
Meniscopathy |
04 |
M |
39 |
182 |
89 |
R |
Meniscopathy |
05 |
M |
41 |
175 |
71 |
R |
Condropathy |
06 |
M |
59 |
169 |
90 |
L |
Meniscopathy |
07 |
M |
27 |
183 |
77 |
L |
Condropathy |
08 |
M |
38 |
167 |
92 |
L |
Arthroscopy of the meniscus |
09 |
M |
51 |
178 |
87 |
L |
Meniscopathy |
10 |
M |
49 |
178 |
84 |
R |
Surgery of meniscus and anterior cruciate ligament |
11 |
M |
36 |
173 |
84 |
L |
Meniscopathy |
12 |
M |
32 |
174 |
70 |
R |
Arthroscopy of the meniscus |
13 |
M |
37 |
185 |
83 |
R |
Arthroscopy of the meniscus |
After the application of US-guided PNM on the femoral nerve, changes were obtained for the mMIS of the quadriceps muscles that had undergone previous pathology. Prior to the intervention, the mean strength was 25.91 kg (SD: 7.17 kg) compared to a mean of 29.98 kg after the intervention (SD: 9.06 kg). The results obtained were statistically significant with a p-value of 0.0019.
It is also important to note that the mMIS of the quadriceps on the healthy contralateral side was 27.59 kg (SD: 7.86 kg), compared to 25.91 kg (SD: 7.17 kg) on the injured side. This finding was statistically significant (p = 0.026) ([Fig. 3]). This data reveals a decrease of the maximal isometric strength on the affected side prior to the intervention. These values, as can be observed in [Fig. 4], after the intervention, are equal or, in many cases, greater than the contralateral measure of the initial reference.




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Discussion
To the best of our knowledge, no study has measured the mMIS of the quadriceps muscle using dynamometry after the application of US-guided PNM in the femoral nerve.
The preintervention measures gathered in the present study reveal that the mean mMIS of the pathological side was 25.91 kg, whereas the mean mMIS of the contralateral side was 27.59 kg. Therefore, there is evidence of weakness of the quadriceps muscle on the leg with a previous injury when compared with the contralateral leg. Nonetheless, according to a systematic review performed by Hart et al, bilateral deficiencies in quadriceps activation are common.[28] This may explain why subjects 6, 8 and 11 presented values in which the mMIS was greater in the leg with previous pathology when compared with the contralateral side.
After the intervention, there was a statistically significant improvement of the mMIS of the quadriceps on the affected side, which increased from a mean of 25.91 kg, prior to the intervention, to 29.98 kg postintervention. This indicates that the PNM was effective for increasing, or hypothetically recovering, the strength of the quadriceps muscles that were inhibited secondary to problems of the joint. The hypothesis regarding this neuromuscular inhibition is a decrease in the corticospinal excitability and/or changes in the spinal reflex.[29]
A systematic review by Sonnery-Cottet et al found moderate evidence for the effectiveness of cryotherapy and physical exercise in the management of muscle inhibition of an articular origin.[30] In contrast, Pietrosimone et al suggested that therapeutic interventions directed at eliciting changes in the voluntary activation of the quadriceps may improve the effectiveness of therapeutic exercise in strength improvements.[31] For this reason, US-guided PNM may be a suitable therapeutic procedure for use prior to exercise programs.
Furthermore, US-guided PNM is a technique that may be employed in patients immediately after either an injury or a surgical intervention, representing a physiotherapy tool that may help prevent the appearance of muscle atrophy and the establishment of neuromuscular inhibition, thus avoiding the negative consequences that may delay or hamper the return to activity of a patient.[29] [32]
This new treatment concept may open new lines of research and provide both the physiotherapist and the patient with improved results regarding strength gains in these types of articular disorders.
The results of the present study reflect preliminary conclusions due to the limitation of the sample size. Future research should confirm these findings and analyze whether similar strength improvements occur in other muscle groups after neural stimulation. Additionally, it is necessary to perform both mid- and long-term assessments of strength using a dynamometer to evaluate how long these improvements are maintained over time.
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Conclusions
Ultrasound-guided PNM has been found to be an effective technique for the reestablishment of isometric strength of the quadriceps in inhibited muscles.
Twitter: @FisioOceano
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Conflicts of Interests
The authors have no conflicts of interests to declare.
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References
- 1 Giles LS, Webster KE, McClelland JA, Cook J. Does quadriceps atrophy exist in individuals with patellofemoral pain? A systematic literature review with meta-analysis. J Orthop Sports Phys Ther 2013; 43 (11) 766-776
- 2 Lewek MD, Rudolph KS, Snyder-Mackler L. Quadriceps femoris muscle weakness and activation failure in patients with symptomatic knee osteoarthritis. J Orthop Res 2004; 22 (01) 110-115
- 3 Vanega Hernández M, Fernández Barrientos O. Rehabilitation of the quadriceps femoris muscle in patients with atrophy after knee post-surgery. Multimed Revista Médica Granma 2018;22(03):
- 4 Hopkins JT, Ingersoll CD. Arthrogenic Muscle inhibition: A Limiting Factor in Joint Rehabilitation. J Sport Rehabil 2000; 9 (02) 135-159
- 5 Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum 2010; 40 (03) 250-266
- 6 McConnell J. Running Injuries: The Infrapatellar Fat Pad and Plica Injuries. Phys Med Rehabil Clin N Am 2016; 27 (01) 79-89
- 7 Henriksen M, Klokker L, Bartholdy C, Graven-Nielsen T, Bliddal H. The Associations between Pain Sensitivity and Knee Muscle Strength in Healthy Volunteers: A Cross-Sectional Study. Pain Res Treat 2013; 2013: 787054
- 8 Otzel DM, Chow JW, Tillman MD. Long-term deficits in quadriceps strength and activation following anterior cruciate ligament reconstruction. Phys Ther Sport 2015; 16 (01) 22-28
- 9 Christensen JC, Mizner RL, Foreman KB, Marcus RL, Pelt CE, LaStayo PC. Quadriceps weakness preferentially predicts detrimental gait compensations among common impairments after total knee arthroplasty. J Orthop Res 2018; 36 (09) 2355-2363
- 10 Meldrum D, Cahalane E, Conroy R, Fitzgerald D, Hardiman O. Maximum voluntary isometric contraction: reference values and clinical application. Amyotroph Lateral Scler 2007; 8 (01) 47-55
- 11 Khamoui AV, Brown LE, Nguyen D. , et al. Relationship between force-time and velocity-time characteristics of dynamic and isometric muscle actions. J Strength Cond Res 2011; 25 (01) 198-204
- 12 West DJ, Owen NJ, Jones MR. , et al. Relationships between force-time characteristics of the isometric midthigh pull and dynamic performance in professional rugby league players. J Strength Cond Res 2011; 25 (11) 3070-3075
- 13 Izquierdo M, Aguado X, Gonzalez R, López JL, Häkkinen K. Maximal and explosive force production capacity and balance performance in men of different ages. Eur J Appl Physiol Occup Physiol 1999; 79 (03) 260-267
- 14 Gorostiaga EM, Izquierdo M, Iturralde P, Ruesta M, Ibáñez J. Effects of heavy resistance training on maximal and explosive force production, endurance and serum hormones in adolescent handball players. Eur J Appl Physiol Occup Physiol 1999; 80 (05) 485-493
- 15 Stone MH, Sands WA, Carlock J. , et al. The importance of isometric maximum strength and peak rate-of-force development in sprint cycling. J Strength Cond Res 2004; 18 (04) 878-884
- 16 Dos'Santos T, Thomas C, Comfort P, McMahon JJ, Jones PA. Relationships between Isometric Force-Time Characteristics and Dynamic Performance. Sports (Basel) 2017; 5 (03) 68
- 17 White JC, Sweet WH. Pain and the neurosurgeon: a forty-year experience. Springfield: Thomas; 1969: 894-9
- 18 Steude U. Percutaneous electro stimulation of the trigeminal nerve in patients with atypical trigeminal neuralgia. Neurochirurgia (Stuttg) 1978; 21 (02) 66-69
- 19 Yakovlev A, Karasev SA, Resch BE, Yakovleva V, Strutsenko A. Treatment of a typical facial pain using peripheral nerve stimulation. Neuromodulation 2011; 14: 553
- 20 McRoberts WP, Cairns K. A retrospective study evaluating the effects of electrode depth and spacing for peripheral nerve field stimulation in patients with back pain. Neuromodulation: Vision 2010. Las Vegas: Proceedings of 14th Annual Meeting of North American Neuromodulation Society; 2010
- 21 Rossi M, DeCarolis G, Liberatoscioli G, Iemma D, Nosella P, Nardi LF. A Novel Mini-invasive Approach to the Treatment of Neuropathic Pain: The PENS Study. Pain Physician 2016; 19 (01) E121-E128
- 22 Rozand V, Grosprêtre S, Stapley PJ, Lepers R. Assessment of Neuromuscular Function Using Percutaneous Electrical Nerve Stimulation. J Vis Exp 2015;(103):
- 23 Minaya Muñoz F, Valera Garrido F. Neuromodulación percutánea ecoguiada. In: Valera Garrido F, Minaya Muñoz F. , editors. Fisioterapia invasiva 2nd ed. Barcelona: Elsevier España, S.L.; 2016: 283-294
- 24 Stauber WT, Barill ER, Stauber RE, Miller GR. Isotonic dynamometry for the assessment of power and fatigue in the knee extensor muscles of females. Clin Physiol 2000; 20 (03) 225-233
- 25 Stam HJ. Dynamometry of the knee extensors; isometric and isokinetic testing in healthy subjects and patients. Erasmus University Rotterdam. 1990 . Available from http://hdl.handle.net/1765/50898
- 26 Anumula SK, Beku C, Murthy YS. Measurement of Reliability in Grip Strength. IPOT 2014; 1 8 (02) 115
- 27 Gustafson KJ, Pinault GCJ, Neville JJ. , et al. Fascicular anatomy of human femoral nerve: implications for neural prostheses using nerve cuff electrodes. J Rehabil Res Dev 2009; 46 (07) 973-984
- 28 Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train 2010; 45 (01) 87-97
- 29 Hobson A. The Etiology of Persistent Quadriceps Weakness Following Anterior Cruciate Ligament Reconstruction. JBJS J Orthop Physician Assist 2018; 6 (03) e24
- 30 Sonnery-Cottet B, Saithna A, Quelard B. , et al. Arthrogenic muscle inhibition after ACL reconstruction: a scoping review of the efficacy of interventions. Br J Sports Med 2018; 53 (05) 289-298
- 31 Pietrosimone BG, Saliba SA. Changes in voluntary quadriceps activation predict changes in quadriceps strength after therapeutic exercise in patients with knee osteoarthritis. Knee 2012; 19 (06) 939-943
- 32 Holder-Powell HM, Di Matteo G, Rutherford OM. Do knee injuries have long-term consequences for isometric and dynamic muscle strength?. Eur J Appl Physiol 2001; 85 (3-4): 310-316
Address for correspondence
-
References
- 1 Giles LS, Webster KE, McClelland JA, Cook J. Does quadriceps atrophy exist in individuals with patellofemoral pain? A systematic literature review with meta-analysis. J Orthop Sports Phys Ther 2013; 43 (11) 766-776
- 2 Lewek MD, Rudolph KS, Snyder-Mackler L. Quadriceps femoris muscle weakness and activation failure in patients with symptomatic knee osteoarthritis. J Orthop Res 2004; 22 (01) 110-115
- 3 Vanega Hernández M, Fernández Barrientos O. Rehabilitation of the quadriceps femoris muscle in patients with atrophy after knee post-surgery. Multimed Revista Médica Granma 2018;22(03):
- 4 Hopkins JT, Ingersoll CD. Arthrogenic Muscle inhibition: A Limiting Factor in Joint Rehabilitation. J Sport Rehabil 2000; 9 (02) 135-159
- 5 Rice DA, McNair PJ. Quadriceps arthrogenic muscle inhibition: neural mechanisms and treatment perspectives. Semin Arthritis Rheum 2010; 40 (03) 250-266
- 6 McConnell J. Running Injuries: The Infrapatellar Fat Pad and Plica Injuries. Phys Med Rehabil Clin N Am 2016; 27 (01) 79-89
- 7 Henriksen M, Klokker L, Bartholdy C, Graven-Nielsen T, Bliddal H. The Associations between Pain Sensitivity and Knee Muscle Strength in Healthy Volunteers: A Cross-Sectional Study. Pain Res Treat 2013; 2013: 787054
- 8 Otzel DM, Chow JW, Tillman MD. Long-term deficits in quadriceps strength and activation following anterior cruciate ligament reconstruction. Phys Ther Sport 2015; 16 (01) 22-28
- 9 Christensen JC, Mizner RL, Foreman KB, Marcus RL, Pelt CE, LaStayo PC. Quadriceps weakness preferentially predicts detrimental gait compensations among common impairments after total knee arthroplasty. J Orthop Res 2018; 36 (09) 2355-2363
- 10 Meldrum D, Cahalane E, Conroy R, Fitzgerald D, Hardiman O. Maximum voluntary isometric contraction: reference values and clinical application. Amyotroph Lateral Scler 2007; 8 (01) 47-55
- 11 Khamoui AV, Brown LE, Nguyen D. , et al. Relationship between force-time and velocity-time characteristics of dynamic and isometric muscle actions. J Strength Cond Res 2011; 25 (01) 198-204
- 12 West DJ, Owen NJ, Jones MR. , et al. Relationships between force-time characteristics of the isometric midthigh pull and dynamic performance in professional rugby league players. J Strength Cond Res 2011; 25 (11) 3070-3075
- 13 Izquierdo M, Aguado X, Gonzalez R, López JL, Häkkinen K. Maximal and explosive force production capacity and balance performance in men of different ages. Eur J Appl Physiol Occup Physiol 1999; 79 (03) 260-267
- 14 Gorostiaga EM, Izquierdo M, Iturralde P, Ruesta M, Ibáñez J. Effects of heavy resistance training on maximal and explosive force production, endurance and serum hormones in adolescent handball players. Eur J Appl Physiol Occup Physiol 1999; 80 (05) 485-493
- 15 Stone MH, Sands WA, Carlock J. , et al. The importance of isometric maximum strength and peak rate-of-force development in sprint cycling. J Strength Cond Res 2004; 18 (04) 878-884
- 16 Dos'Santos T, Thomas C, Comfort P, McMahon JJ, Jones PA. Relationships between Isometric Force-Time Characteristics and Dynamic Performance. Sports (Basel) 2017; 5 (03) 68
- 17 White JC, Sweet WH. Pain and the neurosurgeon: a forty-year experience. Springfield: Thomas; 1969: 894-9
- 18 Steude U. Percutaneous electro stimulation of the trigeminal nerve in patients with atypical trigeminal neuralgia. Neurochirurgia (Stuttg) 1978; 21 (02) 66-69
- 19 Yakovlev A, Karasev SA, Resch BE, Yakovleva V, Strutsenko A. Treatment of a typical facial pain using peripheral nerve stimulation. Neuromodulation 2011; 14: 553
- 20 McRoberts WP, Cairns K. A retrospective study evaluating the effects of electrode depth and spacing for peripheral nerve field stimulation in patients with back pain. Neuromodulation: Vision 2010. Las Vegas: Proceedings of 14th Annual Meeting of North American Neuromodulation Society; 2010
- 21 Rossi M, DeCarolis G, Liberatoscioli G, Iemma D, Nosella P, Nardi LF. A Novel Mini-invasive Approach to the Treatment of Neuropathic Pain: The PENS Study. Pain Physician 2016; 19 (01) E121-E128
- 22 Rozand V, Grosprêtre S, Stapley PJ, Lepers R. Assessment of Neuromuscular Function Using Percutaneous Electrical Nerve Stimulation. J Vis Exp 2015;(103):
- 23 Minaya Muñoz F, Valera Garrido F. Neuromodulación percutánea ecoguiada. In: Valera Garrido F, Minaya Muñoz F. , editors. Fisioterapia invasiva 2nd ed. Barcelona: Elsevier España, S.L.; 2016: 283-294
- 24 Stauber WT, Barill ER, Stauber RE, Miller GR. Isotonic dynamometry for the assessment of power and fatigue in the knee extensor muscles of females. Clin Physiol 2000; 20 (03) 225-233
- 25 Stam HJ. Dynamometry of the knee extensors; isometric and isokinetic testing in healthy subjects and patients. Erasmus University Rotterdam. 1990 . Available from http://hdl.handle.net/1765/50898
- 26 Anumula SK, Beku C, Murthy YS. Measurement of Reliability in Grip Strength. IPOT 2014; 1 8 (02) 115
- 27 Gustafson KJ, Pinault GCJ, Neville JJ. , et al. Fascicular anatomy of human femoral nerve: implications for neural prostheses using nerve cuff electrodes. J Rehabil Res Dev 2009; 46 (07) 973-984
- 28 Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train 2010; 45 (01) 87-97
- 29 Hobson A. The Etiology of Persistent Quadriceps Weakness Following Anterior Cruciate Ligament Reconstruction. JBJS J Orthop Physician Assist 2018; 6 (03) e24
- 30 Sonnery-Cottet B, Saithna A, Quelard B. , et al. Arthrogenic muscle inhibition after ACL reconstruction: a scoping review of the efficacy of interventions. Br J Sports Med 2018; 53 (05) 289-298
- 31 Pietrosimone BG, Saliba SA. Changes in voluntary quadriceps activation predict changes in quadriceps strength after therapeutic exercise in patients with knee osteoarthritis. Knee 2012; 19 (06) 939-943
- 32 Holder-Powell HM, Di Matteo G, Rutherford OM. Do knee injuries have long-term consequences for isometric and dynamic muscle strength?. Eur J Appl Physiol 2001; 85 (3-4): 310-316















