Where your gait might break down.

Gait appears most robust to weakness of hip and knee extensors, which can tolerate weakness well and without a substantial increase in muscle stress. In contrast, gait is most sensitive to weakness of plantarflexors, hip abductors, and hip flexors. - van der Krogt

In the past few weeks I have shared my thoughts on some articles regarding low back paraspinal musculature fatigue and the subsequent effects on motorneuron pools, specifically excitability of the soleus and quadriceps. These shared thoughts are from recent papers in the literature (search the blog over the last week). These effects are suggested to indicate a postural response to preserve lower limb function. In other words, as paraspinal fatigue set in, lower extremity muscle compensation ramped up to sustain postural locomotion demands.  Obviously, one should think this a step further and translate it all into questions of assessment of ankle dorsiflexion (ankle rocker) and control of progressing knee and hip flexion when pertaining to these muscles. The issues of stability and mobility should heighten. The one big problem in these studies, and you have even likely had these thoughts during your clinical examinations, is that one cannot truly fatigue one muscle group alone especially during activity, nor can one assess a single muscle group during manual testing. Luckily we have EMG testing capabilities in this day and age and we can more easily look into the function and reaction of a muscle and its’ direct response reactions. 

Today I have an article by van der Krogt that we read long ago, but that which one of our readers brought back into our wheelhouse.  This is pretty amazing stuff.

“This study examines the extent to which lower limb muscles can be weakened before normal walking is affected. We developed muscle-driven simulations of normal walking and then progressively weakened all major muscle groups, one at the time and simultaneously, to evaluate how much weakness could be tolerated before execution of normal gait became impossible. We further examined the compensations that arose as a result of weakening muscles. Our simulations revealed that normal walking is remarkably robust to weakness of some muscles but sensitive to weakness of others. Gait appears most robust to weakness of hip and knee extensors, which can tolerate weakness well and without a substantial increase in muscle stress. In contrast, gait is most sensitive to weakness of plantarflexors, hip abductors, and hip flexors. Weakness of individual muscles results in increased activation of the weak muscle, and in compensatory activation of other muscles. These compensations are generally inefficient, and generate unbalanced joint moments that require compensatory activation in yet other muscles. As a result, total muscle activation increases with weakness as does the cost of walking.“-van der Krogt

So, if your client comes in with knee, hip or ankle pain and a history of low back pain, you might want to pull out these articles. You may want to consider which muscles are, according to this article, most robust and sensitive to weakness. Remember what I mentioned when i reviewed the soleus article ? I mentioned that the reduced ankle dorsiflexion range may be from a soleus muscle postural compensation reaction to low back pain. Today’s article seemed to confirm that this muscle group is sensitive to weakness. In today’s discussion, not only is the impairment of the hip ranges of motion or control of the knee (from quadriceps adaptive compensation) possibly related to low back pain, in this case, paraspinal fatigue but it may be a muscle group robust to weakness which is a darn good thing when the paraspinals go to nap.

Sometimes the problem is from the bottom up, sometimes it is from the top down. It is what makes this game so challenging and mind numbing at times. If this is all too much for you, in teasing out this quagmire of a system, just throw corrective exercises at your client and hope for the best. What is the worst that can happen if you get it wrong ? Stronger compensations on already present compensations … . . why not, it is good for return business (insert sarcasm emoticon).  But, lets be honest, if it was easy everyone would be doing it the right way. But the truth is that it is a long journey, and we are on the same bus of discovery with you all. 

Dr. Shawn Allen, one of the gait guys.

Reference:

Gait Posture. 2012 May;36(1):113-9. doi: 10.1016/j.gaitpost.2012.01.017. Epub 2012 Mar 3.How robust is human gait to muscle weakness?van der Krogt MM1, Delp SL, Schwartz MH.

Low back pain and quadriceps compensation. A study.

“Neuromuscular changes in the lower extremity occur while resisting knee and hip joint moments following isolated lumbar paraspinal exercise. Persons with a history of LBP seem to rely more heavily on quadriceps activity while jogging.“- Hart et al.

Recently I discussed a paper (link below) about how soleus  motoneuron pool excitability increased following lumbar paraspinal fatigue and how it may indicate a postural response to preserve lower extremity function.
Today I bring you an article of a similar sort.  This paper discusses the plausibility that a relationship exists between lumbar paraspinal muscle fatigue and quadriceps muscle activation and the subsequent changes in hip and knee function when running fatigue ensued. 


"Reduced external knee flexion, knee adduction, knee internal rotation and hip external rotation moments and increased external knee extension moments resulted from repetitive lumbar paraspinal fatiguing exercise. Persons with a self-reported history of LBP had larger knee flexion moments than controls during jogging. Neuromuscular changes in the lower extremity occur while resisting knee and hip joint moments following isolated lumbar paraspinal exercise. Persons with a history of LBP seem to rely more heavily on quadriceps activity while jogging.”- Hart et al.

Whether this or any study was perfectly performed or has validity does not matter in my discussion here today. What does matter pertaining to my dialogue here today is understanding and respecting the value of the clinical examination (and not depending on a gait analysis to determine your corrective exercise prescription and treatment). When an area fatigues and cannot stabilize itself adequately, compensation must occur to adapt. Protective postural control strategies must be attempted and deployed to stay safely upright during locomotion. The system must adapt or pain or injury may ensue, sometimes this may take months or years and the cause is not clear until clinical examination is performed. Your exam must include mobility and stability assessments, motor pattern evaluation, and certainly skill, coordination, ENDURANCE and strength assessments if you are to get a clear picture of what is driving your clients compensation and pain. 

So, if your client comes in with knee, hip or ankle pain and a history of low back pain, you might want to pull out these articles and bash them and other similar ones into your brain. Remember what I mentioned when i reviewed the soleus article ? I mentioned that the reduced ankle dorsiflexion range may be from a soleus muscle postural compensation reaction to low back pain. In today’s discussion, impairment of the hip ranges of motion or control of the knee (from quadriceps adaptive compensation) may also be related to low back pain, in this case, paraspinal fatigue.  

Sometimes the problem is from the bottom up, sometimes it is from the top down. It is what makes this game so challenging and mind numbing at times. If only it were as simple as, “you need to work on abdominal breathing”, or “you need to strengthen your core”.  If only it were that simple. 

Dr. Shawn Allen, one of the gait guys


References:
J Electromyogr Kinesiol. 2011 Jun;21(3):466-70. doi: 10.1016/j.jelekin.2011.02.002. Epub 2011 Mar 8.
Effects of paraspinal fatigue on lower extremity motoneuron excitability in individuals with a history of low back pain. Bunn EA1, Grindstaff TL, Hart JM, Hertel J, Ingersoll CD.

J Electromyogr Kinesiol. 2009 Dec;19(6):e458-64. doi: 10.1016/j.jelekin.2008.09.003. Epub 2008 Dec 16. Jogging gait kinetics following fatiguing lumbar paraspinal exercise.
Hart JM1, Kerrigan DC, Fritz JM, Saliba EN, Gansneder B, Ingersoll CD

Isometrics for patellar tendonitis?We are familiar with different modes of exercise: isometric, isotonic and isokinetic. Isometric exercises have a physiological overflow of 10 degrees on each side of the point of application (ie; to do the exercise…

Isometrics for patellar tendonitis?

We are familiar with different modes of exercise: isometric, isotonic and isokinetic. Isometric exercises have a physiological overflow of 10 degrees on each side of the point of application (ie; to do the exercise at 20 degrees flexion, and you have strength gains from 10 to 30 degrees); isotonics and isokinetics, 15 degrees. Taking advantage of physiological overflow often allows us to bypass painful ranges of motion and still strengthen in that range of motion. 

In this study, they looked at immediate and 45 minute later pain reduction (not function) comparing isometric (max voluntary quadricep contraction) and isotonic (single leg decline squat) exercises. They also looked at cortical inhibition (via the cortico spinal tract) as a result of the exercises. 

Here is what they found: “A single resistance training bout of isometric contractions reduced tendon pain immediately for at least 45 min postintervention and increased MVIC. The reduction in pain was paralleled by a reduction in cortical inhibition, providing insight into potential mechanisms. Isometric contractions can be completed without pain for people with PT. The clinical implications are that isometric muscle contractions may be used to reduce pain in people with PT without a reduction in muscle strength.” These same results were not seen with the isotonic exercise. 

Did the decrease in pain result in the decrease in cortical inhibition (muscle contraction is inhibited across an inflamed joint: Rice, McNair 2010; Iles, Stokes 1987)? Was it a play on post isometric inhibition (most likely not, since this usually only lasts seconds to minutes post contraction) ? Or is there another mechanism at play here? There has been one other paper we found here, that shows cortical inhibition of quadriceps post isometric exercise. Time will tell. In the meantime, start using those multiple angle isometrics!

The Gait Guys

Rio E, Kidgell D, Purdam C, Gaida J, Moseley GL, Pearce AJ, Cook J.Isometric exercise induces analgesia and reduces inhibition in patellar tendinopathy Br J Sports Med. 2015 May 15. pii: bjsports-2014-094386. doi: 10.1136/bjsports-2014-094386. [Epub ahead of print]

http://www.anatomy-physiotherapy.com/28-systems/musculoskeletal/lower-extremity/knee/1163-isometric-exercises-in-patellar-tendinopathy

Can the VMO be selectively activated?

They have a common nerve innervation, so many studies say no. Perhaps altering internal/external orientation of the lower extremity (1) or joint angles (2) may play a role. Of course, it also depends on how you are measuring (3). Intramuscular seems to be most accurate!

In the Link Below, section 4, is a nice, brief review of the literature. Thanks to Daithi Grey for the inspiration to put this up!

1. J Strength Cond Res. 2014 Sep;28(9):2536-45. doi: 10.1519/JSC.0000000000000582.
Range of motion and leg rotation affect electromyography activation levels of the superficial quadriceps muscles during leg extension.Signorile JF1, Lew KM, Stoutenberg M, Pluchino A, Lewis JE, Gao J.

2. Phys Ther Sport. 2013 Feb;14(1):44-9. doi: 10.1016/j.ptsp.2012.02.006. Epub 2012 Jun 26.
Muscle activation of vastus medialis obliquus and vastus lateralis during a dynamic leg press exercise with and without isometric hip adduction. Peng HT1, Kernozek TW, Song CY.

3. J Electromyogr Kinesiol. 2013 Apr;23(2):443-7. doi: 10.1016/j.jelekin.2012.10.003. Epub 2012 Nov 8.
The VMO:VL activation ratio while squatting with hip adduction is influenced by the choice of recording electrode. Wong YM1, Straub RK, Powers CM.


http://www.mikereinold.com/2009/05/10-principles-of-patellofemoral.html

10 Principles of Patellofemoral Rehabilitation - Mike Reinold

“Emphasize the QuadricepsThe next principle of patellofemoral rehabilitation is to strengthen the knee extensor musculature. Some authors have recommended emphasis on enhancing the activation of the VMO in patellofemoral patients based on reports of isolated VMO insufficiency and asynchronous neuromuscular timing between the VMO and VL.While the literature offers conflicted reports on selective recruitment and neuromuscular timing of the vasti musculature, the VMO may have a greater biomechanical effect on medial stabilization of the patella than knee extension due to the angle of pull of the muscle fibers at approximately 50-55 degrees.  Wilk et al(JOSPT 1998) suggest that the VMO should only be emphasized if the angle of insertion of the VMO on the patella is in a position in which it may offer a certain degree of dynamic or active lateral stabilization.  As you can see by the figure, if the fibers are not aligned in a position to assist with patellar stabilization, VMO training will likely not be effective.  This orientation of the muscle fibers will differ from patient to patient and can be visualized.Several interventions and exercise modifications have been advocated to effectively increase the VMO:VL ratio, based mostly on anecdotal observations. These include hip adduction, internal tibial rotation, and patellar taping and bracing. Powers(JOSPT 1998) reports that isolation of VMO activation may not be possible during exercise, stating that several studies have shown that selective VMO function was not found during quadriceps strengthening exercises, exercises incorporating hip adduction, or exercises incorporating internal tibial rotation. Powers also states that although the literature offers varying support for VMO strengthening, successful clinical results have been found while utilizing this treatment approach.My belief is that quadriceps strengthening exercises should be incorporated into patellofemoral rehabilitation programs. Strength deficits of the quadriceps may lead to altered biomechanical properties of the patellofemoral and tibiofemoral joints. Any change in quadriceps force on the patella may modify the resultant force vector produced by the synergistic pull of the quadriceps and patellar tendons, thus altering contact location and pressure distribution of joint forces. Furthermore, the quadriceps musculature serves as a shock absorber during weightbearing and joint compression, any abnormal deviations in quadriceps strength may result in further strain on the patellofemoral and/or tibiofemoral joint.In reality, I believe that quadriceps strengthening is very important for patellofemoral rehabilitation, but many exercises designed to “enhance VMO” strength or activation may actually be disadvantageous to the joint.  Take for example the classic squeezing of the ball during closed kinetic chain exercises such as squatting and leg press.  This creates an IR and adduction moment at the hip that is now known to be detrimental to patellofemoral patients.  I would actually propose that we work on quadriceps strengthening without an adduction component and rather emphasize hip adbuction and external rotation.  This can be performed with the use of a piece of exercise band around the patient’s knees during these exercises. “

Lombard's Paradox: A unique look at the cooperation of the quadriceps and hamstrings

Lombard’s Paradox

 In searching our personal archives for neat stuff we came across an oldie but a goodie. We posted this one on the blog for the first time in July 2011 so it was time to revisit it here on the blogs “Rerun Fridays”. This is one to certainly make your head spin. We do not even know where this came from and how much was our original material and how much was someone  else’s.  If you can find the reference we would love to give it credit.  We do now that we added some stuff to this but we don’t even know what parts were ours !  Regardless, there is a brain twister here worth juggling in your heads.  Lets start with this thought……..

When you are sitting the rectus femoris (a quad muscle) is “theoretically” shortened because the hip is in flexion. It crosses the bent knee in the front at it blends with the patellar tendon, thus it is “theoretically” lengthened at the knee.  When we stand up, the hip extends and the knee extends, making the R. Femoris “theoretically” lengthen at the hip and shorten at the knee.  This, it bodes the question…….did the R. Femoris even change length at all ? And the hamstrings kind of go through the same phenomenon. It is part of the  uniqueness of “two joint” muscles.   Now, onto Lombard’s paradox with more in depth thought on this topic.

Warren Plimpton Lombard (1855-1939) sought to explain why the quadriceps and hamstring muscles contracted simultaneously during the sit-to-stand motion.  He noted that the rectus femoris and the hamstrings are antagonistic, and this coactivation is known as Lombard’s paradox.

The paradox is classically explained by noting the relative moment arms of the hamstrings and rectus femoris at either the hip or the knee, and their effects on the magnitude of the moments produced by either muscle group at each of the two joints.

By virtue of the fact that muscles cannot develop different amounts of force in their different parts, the paradox develops.  The hamstrings cannot selectively extend the hip without imparting an equal force at the knee. Thus, the only way for hip extension and knee extension to occur simultaneously in the act of standing (or eccentrically in the act of sitting) is for the net moment to be an extensor moment at both the hip and knee joints. Lombard suggested three necessary conditions for such paradoxical co-contraction:

  • the lever arm of the muscle must be greater at its extensor end
  • a two-joint muscle must exist with opposite function
  • the muscle must have sufficient leverage so as to use the passive tendon properties of the other muscle

In 1989, Felix Zajac & co-workers pointed out that the role of muscles, particularly two-joint muscles, was much more complex than has traditionally been assumed. For example, in certain situations, the gastrocnemius could act as a knee extensor. It is clear now that the direction in which a joint is accelerated depends on the dynamic state of all body segments, making it difficult to predict the effect of an individual muscle contraction without extensive and accurate biomechanical models (Zajac et al, 2003).

 In fact, back to the gastrocnemius another 2+ joint muscle (crosses knee, mortise and subtalar joints), we all typically think of it as a “push off” muscle.  It causes the heel to rise and accelerates push off in gait and running. But, when the foot is fixed on the ground the insertion is more stable and thus the contraction, because the origin is above the posterior joint line, can pull the femoral condyles into a posterior shear vector. It thus, like the hamstrings, needs to be adequately trained in a ACL or post-operative ACL, deficient knee to help reduce the anterior shear of normal joint loading. It is vital to note, that when ankle rocker is less than 90  degrees (less than 90 degrees of ankle dorsiflexion is available), knee hyperextension is a viable strategy to progress forward in the sagittal plane.  But in this scenarios, the posterior shear capabilites of the gastrocnemius are brought to the front of the line as a frequent strategy.  And not a good one for the menisci we should mention.

Andrews J G (1982)  On the relationship between resultant joint torques and muscular activity  Med Sci Sports Exerc  14: 361-367.

Andrews J G (1985)  A general method for determining the functional role of a muscle  J Biomech Eng  107: 348-353.

Bobbert MF, van Soest AJ (2000) Two-joint muscles offer the solution - but what was the problem? Motor Control 4: 48-52 & 97-116.

Gregor, R.J., Cavanagh, P.R., & LaFortune, M. (1985). Knee flexor moments during propulsion in cycling—a creative solution to Lombard’s Paradox. Journal of Biomechanics, 18, 307-16 .

Ingen-Schenau GJv (1989) From rotation to translation: constraints on multi-joint movement and the unique action of bi-articular muscles. Hum. Mov. Sci. 8:301-37.

Lombard, W.P., & Abbott, F.M. (1907). The mechanical effects produced by the contraction of individual muscles of the thigh of the frog. American Journal of Physiology, 20, 1-60.

Mansour J M & Pereira J M (1987)  Quantitative functional anatomy of the lower limb with application to human gait  J Biomech  20: 51-58.

Park S, Krebs DE, Mann RW (1999) Hip muscle co-contraction: evidence from concurrent in vivo pressure measurement and force estimation. Gait & Posture 10: 211-222.

Rasch, P.J., & Burke, R.K. (1978). Kinesiology and applied anatomy. (6th ed.). Philadelphia: Lea & Febiger.

Visser JJ, Hoogkamer JE, Bobbert MF & Huijing PA (1990) Length and Moment Arm of Human Leg Muscles as a Function of Knee and Hip Angles. Eur. J Appl Physiol 61: 453-460.

Zajac FE & Gordon MF (1989) Determining muscle’s force and action in multi-articular movement  Exerc Sport Sci Revs  17: 187-230.

Zajac FE, Neptune RR, Kautz SA (2003) Biomechanics and muscle coordination of human walking - Part II: Lessons from
dynamical simulations and clinical implications, Gait & Posure 17 (1): 1-17.

A tangled tail of two, 2-joint muscles: Lombard’s Paradox

Two years ago we wrote this little piece on these 2 two joint muscles.  Their companionship mentally came up during the sorting out of a strange client case so we felt it was good karma to share it again.   This one may make your head spin.

We do not know where this write up came from and how much was our original material and how much was someone else’s. It was found on an old computer of long ago. If you can find the reference we would love to give it credit.  We do know that we added some stuff to this but we don’t even know what parts were ours !  Regardless, there is a brain twister here worth juggling in your heads.  Some of it we know is far reaching and even marginally incorrect, but we like mental aerobics to take it for what its worth. There is value in thinking about things this way. Lets start with this thought……..

When you are sitting the rectus femoris (a quad muscle) is “theoretically” shortened at the hip because the hip is in flexion. It also  crosses the bent knee in the front at it blends with the patellar tendon, thus it is “theoretically” lengthened at the knee.  When we stand up, the hip extends and the knee extends, making the R. Femoris “theoretically” lengthen at the hip and shorten at the knee.  Thus, it bodes the question…….did the R. Femoris even change length at all ? Did a concentric event occur at one end and an eccentric contractile event occur at the other ? Is that even possible ? And, the hamstrings kind of go through the same phenomenon on the other side of the knee and hip so you possibly have a very complex dialogue across the front and the back of the knee and hip during movement. And for every angle of flexion or extension change around the knee or hip both the quads and the hamstrings have this sliding scale of change they have to play, it should be a perfect give and take phenomenon. And when orchestrated cleanly the joints do not see impairment. This is part of the uniqueness of “two joint” muscles.  However, think about how a short quadriceps, a very common clinical finding, will impair this orchestra. Like an instrument out of tune the orchestration is in flux and alternative strategies ensue. How will the function at the knee be changed by this short quadriceps ? How will hip extension be impaired ?  How will the hamstring alter its function ? What will the consequences be ? What alternative motor patterns will be deployed ? And if you are just doing your gait analysis without a clinical examination what will you see as their compensation ? Now that your head is buzzing, onto Lombard’s paradox with more in depth thought on this topic.

Warren Plimpton Lombard (1855-1939) sought to explain why the quadriceps and hamstring muscles contracted simultaneously during the sit-to-stand motion.  He noted that the rectus femoris and the hamstrings are antagonistic, and this coactivation is known as Lombard’s paradox.

The paradox is classically explained by noting the relative moment arms of the hamstrings and rectus femoris at either the hip or the knee, and their effects on the magnitude of the moments produced by either muscle group at each of the two joints.

By virtue of the fact that muscles cannot develop different amounts of force in their different parts, the paradox develops.  The hamstrings cannot selectively extend the hip without imparting an equal force at the knee. Thus, the only way for hip extension and knee extension to occur simultaneously in the act of standing (or eccentrically in the act of sitting) is for the net moment to be an extensor moment at both the hip and knee joints. Lombard suggested three necessary conditions for such paradoxical co-contraction:

  • the lever arm of the muscle must be greater at its extensor end
  • a two-joint muscle must exist with opposite function
  • the muscle must have sufficient leverage so as to use the passive tendon properties of the other muscle

In 1989, Felix Zajac & co-workers pointed out that the role of muscles, particularly two-joint muscles, was much more complex than has traditionally been assumed. For example, in certain situations, the gastrocnemius could act as a knee extensor. It is clear now that the direction in which a joint is accelerated depends on the dynamic state of all body segments, making it difficult to predict the effect of an individual muscle contraction without extensive and accurate biomechanical models (Zajac et al, 2003).

 In fact, back to the gastrocnemius another 2+ joint muscle (crosses knee, mortise and subtalar joints), we all typically think of it as a “push off” muscle.  It causes the heel to rise and accelerates push off in gait and running. But, when the foot is fixed on the ground the insertion is more stable and thus the contraction, because the origin is above the posterior joint line, can pull the femoral condyles into a posterior shear vector. It thus, like the hamstrings, needs to be adequately trained in a ACL or post-operative ACL, deficient knee to help reduce the anterior shear of normal joint loading. It is vital to note, that when ankle rocker is less than 90  degrees (less than 90 degrees of ankle dorsiflexion is available), knee hyperextension is a viable strategy to progress forward over the ankle in the sagittal plane.  But in this scenario, the posterior shear capabilites of the gastrocnemius are brought to the front of the line as a frequent strategy.  And not a good one for the menisci we should mention.

Just some random thoughts for you today. We used to play such mental games during my orthopedic residency. The “what would happen if” scenarios. They stimulate thought, dialogue and debate and get the brain thinking more globally.  We hope you enjoyed the circus show today !

Shawn and Ivo…….. the gait guys

Andrews J G (1982)  On the relationship between resultant joint torques and muscular activity  Med Sci Sports Exerc  14: 361-367.

Andrews J G (1985)  A general method for determining the functional role of a muscle  J Biomech Eng  107: 348-353.

Bobbert MF, van Soest AJ (2000) Two-joint muscles offer the solution - but what was the problem? Motor Control 4: 48-52 & 97-116.

Gregor, R.J., Cavanagh, P.R., & LaFortune, M. (1985). Knee flexor moments during propulsion in cycling—a creative solution to Lombard’s Paradox. Journal of Biomechanics, 18, 307-16 .

Ingen-Schenau GJv (1989) From rotation to translation: constraints on multi-joint movement and the unique action of bi-articular muscles. Hum. Mov. Sci. 8:301-37.

Lombard, W.P., & Abbott, F.M. (1907). The mechanical effects produced by the contraction of individual muscles of the thigh of the frog. American Journal of Physiology, 20, 1-60.

Mansour J M & Pereira J M (1987)  Quantitative functional anatomy of the lower limb with application to human gait  J Biomech  20: 51-58.

Park S, Krebs DE, Mann RW (1999) Hip muscle co-contraction: evidence from concurrent in vivo pressure measurement and force estimation. Gait & Posture 10: 211-222.

Rasch, P.J., & Burke, R.K. (1978). Kinesiology and applied anatomy. (6th ed.). Philadelphia: Lea & Febiger.

Visser JJ, Hoogkamer JE, Bobbert MF & Huijing PA (1990) Length and Moment Arm of Human Leg Muscles as a Function of Knee and Hip Angles. Eur. J Appl Physiol 61: 453-460.

Zajac FE & Gordon MF (1989) Determining muscle’s force and action in multi-articular movement  Exerc Sport Sci Revs  17: 187-230.

Zajac FE, Neptune RR, Kautz SA (2003) Biomechanics and muscle coordination of human walking - Part II: Lessons from
dynamical simulations and clinical implications, Gait & Posure 17 (1): 1-17.