Effect of Vastus Medialis Loss on Rabbit Patellofemoral Joint Contact Pressure Distribution

in Journal of Applied Biomechanics
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  • 1 University of Calgary
  • 2 Federal University of Santa Catarina

Vastus medialis (VM) weakness is thought to alter patellar tracking, thereby changing the loading of the patellofemoral joint (PFJ), resulting in patellofemoral pain. However, it is challenging to measure VM force and weakness in human studies, nor is it possible to measure the associated mechanical changes in the PFJ. To obtain fundamental insight into VM weakness and its effects on PFJ mechanics, the authors determined PFJ loading in the presence of experimentally simulated VM weakness. Skeletally mature New Zealand White rabbits were used (n = 6), and the vastus lateralis, VM, and rectus femoris were stimulated individually through 3 custom-built nerve cuff electrodes. Muscle torque and PFJ pressure distribution were measured while activating all muscles simultaneously, or when the vastus lateralis and rectus femoris were activated, while VM was not, to simulate a quadriceps muscle strength imbalance. For a given muscular joint torque, peak pressures were greater and joint contact areas were smaller when simulating VM weakness compared with the condition where all muscles were activated simultaneously. The results in the rabbit model support that VM weakness results in altered PFJ loading, which may cause patellofemoral pain, often associated with a strength imbalance of the knee extensor muscle group.

Patellofemoral pain is defined as anterior knee pain or retro patellar pain,1,2 and it is often described as one of the most common musculoskeletal disorders.3 Incident rates for patellofemoral pain were reported, ranging from 12% to 17% of all knee-related injuries,36 affecting a large spectrum of the population, including a general, nonspecific group,7,8 physically active people,4,9 young/adolescents,8,10,11 and older adults.12 It has been suggested that patellofemoral pain may potentially lead to osteoarthritis in the patellofemoral joint (PFJ).1315 Despite the frequent occurrence and clinical importance of patellofemoral pain, its etiology remains unclear.

A frequently implicated cause for patellofemoral pain is quadriceps muscle weakness and imbalance, specifically weakness of the vastus medialis (VM).1618 The VM is thought to be a medial stabilizer of the patella,19,20 thus contributing to the proper function of the PFJ. Electromyography of the individual quadriceps muscles has led to the suggestion that a delayed onset of VM2124 and a lower magnitude of VM activation25 may be a cause of patellofemoral pain. Based on these results and similar other findings, it has been assumed that VM weakness causes increased PFJ contact pressures over smaller joint contact areas, which might lead to patellofemoral pain.

There have been a few attempts at determining the relationship between VM weakness and PFJ pressure distribution. However, it is impossible to derive decisive conclusions from these studies due to fundamental experimental limitations. For example, in several studies, human cadaveric specimens were used to determine changes in PFJ pressure distribution, using experimentally simulated VM weakness.20,2628 In these studies, the quadriceps muscles were represented by wires pulling in the direction of the muscle fibers as they insert into the patella. However, it is trivial to show that the line of action of pennate muscles, such as the VM and vastus lateralis (VL), is not along the distal muscle fiber direction, but along a line connecting origin and insertion. Thus, the medial and lateral forces of VM and VL on the patella simulated by wires along the distal fiber direction did not represent the actual forces and lines of action of these muscles. In order to overcome the limitations associated with some experimental approaches using human cadavers, computational approaches were introduced and combined with in vitro research.29 Using such an approach, it was found that a decrease in VM force resulted in increased lateral pressure and decreased medial pressure in human PFJs.29 These computational results agreed with the results obtained experimentally, establishing a theoretical approach that can be used to estimate changes in patellofemoral pressure distributions in the case of VM weakness. However, as the detailed geometries of human knee joints and associated muscles are specific to each person, and as it is virtually impossible to obtain accurate estimates of human VM weakness in vivo, computational approaches also have their limitations. In an animal study, in which the quadriceps muscles were activated by femoral nerve stimulation, VM weakness was simulated by transecting the VM in midbelly. Prior to and following the VM transection, muscle force and PFJ pressure measurements were directly measured for comparable joint loads.30 However, in that study, they did not account for the fact that the VM is innervated in its proximal third. Therefore, cutting the VM in midbelly might still have allowed for VM innervation and VM force transmission through intermuscular connections,31 thereby contributing to the PFJ pressure distribution. Furthermore, pressure distributions in that study were only measured for pressures exceeding 2.5 MPa, thereby ignoring low pressure areas that might be crucial in the understanding of PFJ mechanics.

Recently, we developed a new experimental approach that allows for independent control and activation of the individual quadriceps muscles in the rabbit hind limb.32 Using this approach, it is possible to simulate any muscle imbalance and coordination pattern of the quadriceps muscle, while simultaneously measuring the quadriceps forces and corresponding PFJ pressure distributions. Because of the presumed importance of VM weakness in patellofemoral pain, the purpose of this study was to determine the effect of VM loss on PFJ pressure distribution. We hypothesized that VM weakness is associated with increased peak pressures and decreased PFJ contact areas for precisely matched knee extensor forces.

Methods

Animals and Surgery

Experiments were performed on skeletally mature New Zealand White rabbits (n = 6, 1 y old, 3.9 [0.5] kg; Covance Inc, Princeton, NJ). The rabbits were tranquillized with 1 mL/kg with Acevet (25 mg/mL; Vetoquinol NA. Inc, Lavaltrie, QC, Canada) and held under anesthesia with a 2% isoflurane/oxygen mixture during the experiment, while vital signs were monitored and maintained throughout the experiment. After the experiment, the animals were euthanized with an overdose injection of Euthanyl (MTC Pharmaceuticals, Cambridge, ON, Canada) into the lateral ear vein.

Three home-built nerve cuff electrodes were surgically implanted on the nerve branches of the VL, VM, and rectus femoris (RF) for controlled individual stimulation of these muscles.32 Then, a medial and lateral retinacular incision were made to allow for the insertion of a pressure-sensitive film between the patella and the femoral groove.30,33 All muscles crossing the knee and all knee ligaments were preserved.

All experimental procedures and protocols were approved by the Animal Care Committee of the University of Calgary (IDNo AC 16-0028).

Quadriceps Muscle Activation and Knee Extensor Force Calculation

After the completion of all surgical procedures, the rabbits were fixed in a custom-built, stereotaxic frame using bilateral bone pins inserted into the iliac fossa and the femoral condyles.34,35 A servomotor (Parker Hannifin Corporation, Irwin, PA), controlled by user-defined software (Motion Planner, Rohnert Park, CA), was used to hold the experimental leg at a 90° knee joint angle. Great care was taken to align the axis of the knee with the rotational axis of the servomotor by testing for movements of the shank along the motor shaft when the knee was led through its full range of motion.

To activate the quadriceps muscle group individually, VL, VM, and RF were stimulated through each nerve cuff using 2 dual-channel stimulators (Grass S8800; Astro/Med Inc, Longueuil, QC, Canada). The stimulation voltage was set to a level twice that of the motor unit threshold level to ensure that all motor units of each muscle were recruited.33,34,36 Once the recruitment of all motor units had been achieved, the stimulation frequencies were changed from 35 Hz to 100 Hz (maximum force), using 1 to 2 Hz increments in order to produce different levels of muscle activation and corresponding changes in muscle force. In order to simulate VM weakness experimentally, 2 conditions were analyzed specifically: in the first condition, all 3 muscles (VL, VM, and RF) were stimulated simultaneously (ALL), and in the second condition, only the VL and RF were stimulated simultaneously (VLRF), while the VM was kept passive. A 2-minute rest period was given between contractions to limit muscle fatigue. Stimulating the quadriceps muscles in this manner resulted in many “force-matched” pairs, where different muscles stimulated at different frequencies produced similar knee extensor forces (5% difference). These force-matched pairs were later identified and used for comparison of the joint loading when knee extensor forces were similar for the ALL and VLRF conditions.

Knee extensor torques were measured using a custom-built torque sensor (Vishay 2100 amplifier; Vishay Precision Group, Wendell, NC), and data were collected using Windaq software (collection card, DI-400, 12 bit; DAQ Instruments, Akron, OH, US). The quadriceps moment arm was approximated by measuring the distance from the midsection of the patellar tendon to the joint center.30 The knee extensor force was then determined by dividing the measured knee extensor torques by the corresponding moment arm length.

PFJ Contact Pressure Measurements and Analysis

Three different types of pressure sensitive films (Fuji prescale film; Fuji Photo Film Co. Ltd, Tokyo, Japan) were used to measure PFJ pressures: super low sensitive (pressure range: 0–2.5 MPa), low sensitive (2.5–10 MPa), and medium sensitive film (10–50 MPa). The films were cut into 1-cm wide and 10-cm long strips sealed with a thin adhesive tape to keep the films dry.33 The thickness of the strips was 0.3 mm for the super-low– and low-type films, and 0.2 mm for the medium sensitive film. In order to insert the film, the experimental leg was extended and the film was inserted through the retinacular incisions of the PFJ. Then, the knee joint angle was set and held at 90° by the servomotor. Typically, pressure distribution was measured by using all 3 types of pressure sensitive films to capture the entire joint contact area (super low sensitive film), and also capture the peak pressures without saturation (low and medium sensitive films).

Pressure stains from the pressure sensitive films were digitized by scanning them at a spatial resolution of 0.04 mm. Then, the resulting images were converted into grayscale images of 256 levels of intensity. Peak pressures were defined as the highest average pressure measured over a region of 0.25 mm2, and joint contact areas were calculated by the number of pixels with stain. Peak pressures and joint contact areas were analyzed using custom-written MATLAB program (The MathWorks, Natick, MA).

In order to convert the pressure stains into actual pressure values, the 3 types of pressure-sensitive films were calibrated using a materials-testing machine. A flat, circular indenter of radius 1 mm was pressed against the pressure-sensitive films using forces that covered the entire range of measurement. Nine calibration stains for the super low film (0–2.6 MPa), 13 calibration stains for the low film (1.3–14.2 MPa), and 18 calibration stains for the medium film (10.4–54.4 MPa) were used to derive the calibration curves.

Statistics

Wilcoxon signed-rank tests were used to compare the peak pressures and joint contact areas for the matched force trials between the ALL and VLRF conditions. The level of significance was set at P < .05, and all descriptive results are presented as means (1 SD).

Results

Representative raw pressure data of joint contact areas and corresponding contact forces for the ALL and VLRF conditions are shown in Table 1. Muscle force (in percentage) was normalized to the maximum force (100 Hz activation), when all muscles were stimulated simultaneously. The actual muscle force (in Newton) and contact area (in millimeters squares) for each pressure stain are shown. The top and bottom of each pressure image represent the proximal and distal ends of the PFJ, while the left and right sides indicate the medial and lateral sides of the PFJ, respectively. Note that the joint contact shapes of ALL and VLRF are distinctly different.

Table 1

Representative Results for 5 Force-Matched Pairs From One Animal

Normalized force, %ALLVLRF
10
27.9 N28.3 N
5.4 mm23.3 mm2
18
48.0 N46.4 N 
10.1 mm29.8 mm2 
26 
70.0 N72.5 N 
13.8 mm213.1 mm2 
33 
90.4 N86.9 N 
16.0 mm215.2 mm2 
45 
118.5 N115.4 N 
17.5 mm216.8 mm2 

Abbreviations: ALL, VL, VM, and RF were stimulated simultaneously; VLRF, only the VL and RF were stimulated simultaneously.

The data from one animal were excluded from the results due to damage to the nerve branch innervating RF. For the peak pressure comparisons, 49 force-matched trials (4, 8, 6, 18, and 13 trials in each animal) across a wide range of knee extensor forces were identified from all tested animals and were used for subsequent analysis. The mean peak pressure for the VLRF (34.9 [18.0] MPa) was 20.7% higher compared with the ALL condition (28.9 [16.0] MPa, Figure 1A, P < .001).

Figure 1
Figure 1

—Peak pressures (A) and contact areas (B) for the ALL and VLRF conditions. Peak pressures were greater and joint contact areas were smaller for the VLRF compared with the ALL condition. Open circles represent individual data points, and corresponding force matched pairs are connected by a thin dashed line. The short, horizontal bars indicate the mean values for each condition, and the long, vertical bars show ±1 SD from the mean. ALL indicates vastus lateralis (VL), vastus medialis, and rectus femoris (RF) were stimulated simultaneously; VLRF, only the VL and RF were stimulated simultaneously. Asterisks indicate statistical difference between the ALL and VLRF conditions (P < .05).

Citation: Journal of Applied Biomechanics 36, 6; 10.1123/jab.2020-0056

Twenty-nine force-matched trials (1, 2, 6, 13, 7 trials in each animal) were identified from the super low sensitive film for comparison of PFJ contact areas across a wide range of knee extensor forces. The PFJ contact areas in the VLRF (11.6 [4.6] mm2) were 4% smaller relative to the condition ALL (12.1 [4.8] mm2, Figure 1B, P = .020).

Since force-matched pairs were obtained across a large range of muscle force, peak pressures and joint contact areas varied considerably, resulting in high SD values. However, the Wilcoxon signed-rank tests eliminate these variations by making comparisons across the force-matched pairs, thus giving statistically significant observations.

Discussion

The purpose of this study was to determine the effects of quadriceps muscle imbalance on PFJ pressure distribution. Specifically, we quantified the effects of a complete loss of VM function by comparing peak pressures and contact areas in the PFJ when the quadriceps muscles were activated with and without VM. The primary result of this study was that the loss of VM was associated with increased peak pressures and reduced PFJ contact areas for conditions where the quadriceps forces and the knee joint angle were matched, and hence, the same amount of force was transferred across the PFJ.

Our results support previous studies on human cadaveric specimens that found decreased joint contact areas with a loss or a decrease in the force of VM,20,26,28 and also support computational approaches of human PFJ pressure distributions with VM weakness.29 Combined, these results may suggest a scenario whereby VM weakness causes an abnormal pressure distribution, which might result in patellofemoral pain. However, as mentioned previously, in the human cadaveric studies, the quadriceps muscles were represented by pulleys and cables pulling in the direction of distal muscle fiber insertion into the patella. This results in substantial medial and lateral force components of the VM and VL muscles, respectively, on the patella. Needless to say, such a representation of the VM and VL is simplified and does not reflect the actual lines of action of these muscles, which go through the origin and insertion sites of the individual muscles.

Quadriceps muscle weakness in rabbits, induced by injections of botulinum toxin type A, has been found to be associated with the onset of knee osteoarthritis at 1 to 3 months postweakness induction.3739 Quadriceps muscle strength imbalance, simulated experimentally by unilateral denervation of the VL, also resulted in significantly higher, histologically assessed osteoarthritis scores in the experimental compared with the control limb at 3 months postintervention.38 These results may, in part, be a reflection of increasing peak pressures with the weakness of VL and quadriceps muscle strength imbalance. More likely, however, the onset and progression of osteoarthritis in the PFJ of rabbits may reflect altered use and activation patterns of the quadriceps muscles in the presence of weakness and imbalance.

Quadriceps muscle weakness has been associated with human knee osteoarthritis in some studies,14,40,41 but not in others.13 Therefore, quadriceps weakness is thought to be a weak predictor of knee osteoarthritis at best.42 There are several reasons for the contrary results between knee extensor weakness and knee osteoarthritis in humans. Measuring muscle strength in humans using voluntary contractions is unreliable,43 and this situation appears confounded when asking patients with knee pain to produce maximal muscle forces. Furthermore, it is difficult to normalize muscle forces across subjects and within subjects, and most difficult to normalize them for comparison between patients with knee OA and healthy control subjects.44 For these reasons, human studies aimed at investigating the relationship between knee joint pain, patellofemoral pain, osteoarthritis, and muscle weakness/strength imbalance are hard to conduct, and technological development that allows for the accurate identification of muscle imbalances and changes in joint contact distribution patterns needs to be developed before satisfactory progress in this area can be made.

In a previous study, in which the effects of VM weakness on rabbit PFJ mechanics were simulated by surgically transecting the VM in midbelly, VM weakness did not cause changes in PFJ pressure distributions.30 Specifically, Sawatsky et al found that peak pressures and joint contact areas were the same prior to and following the VM transection for force-matched test conditions. This result contradicts our findings of increased peak pressures and decreased joint contact areas in the presence of VM weakness. There are several methodological differences between the 2 studies that might explain the discrepancies in the results. First of all, in the previous study, the joint contact areas were determined using the low pressure sensitive film only, which has a pressure threshold of 2.5 MPa; therefore, the contact areas with a pressure of <2.5 MPa were ignored. In our study, all joint contact area measurements were obtained using the super low sensitive film, which has a negligible pressure threshold, providing contact areas that include pressures below 2.5 MPa. Therefore, the difference in the contact area results between the 2 studies may be associated with the joint contact areas that are comprised of pressure values below 2.5 MPa. Second, the quadriceps muscles in the previous study were activated via femoral nerve stimulation, and VM weakness was simulated by transecting the VM in midbelly. The motor endplate for the rabbit VM is in the proximal third of the muscle; therefore, the proximal part of the VM may still have been activated following muscle transection, contributing to the knee extensor forces, through intermuscular pathways.31,45,46 Intermuscular force transmission from the VM to other quadriceps muscles was not possible in the current study, as VM was not activated. Third, we did not activate the vastus intermedius muscle, while Sawatsky et al30 activated vastus intermedius with the other quadriceps muscles. As VL and VM are thought to be the primary lateral and medial stabilizer of the patella,18 not activating the vastus intermedius would not be expected to affect our results, but nevertheless, cannot be ruled out.

Even though the detailed anatomy of the quadriceps muscle group and the PFJ differs between humans and rabbits, they are remarkably similar. Important for the current study, the VM inserts into the patella at its medial border, with a fiber direction of the distal part of the VM that is at a distinct angle of 50° to 55°  in humans and 45° to 50°  in rabbits,30 relative to the long axis of the femur. Because of this anatomical configuration, the VM has been considered a medial stabilizer of the patella in human and rabbit knees. In human studies, it has been reported that VM weakness produces a lateral shift of the patella relative to the femoral groove.1618,22 This lateral shift of the patella is thought to cause higher contact stresses and smaller joint contact areas,47 which has been associated with patellofemoral pain. A lateral shift of the patella in cadaveric specimens has also been shown to cause a decrease in the PFJ contact area,26,27,48 with a shift of the contact area toward the lateral facet of the patella.27 These studies support the present results, regardless of the anatomical differences of the quadriceps muscles and the PFJ between rabbits and humans.

A limitation of the current study was that all test procedures were performed nonweight bearing, while weight bearing might affect the orientation of the tibia relative to the femur, and thus, it might be a modulator of PFJ mechanics.49 Also, inserting the pressure-sensitive film into the PFJ is associated with a small change in the PFJ mechanics,50 but this is a systematic error that would likely not affect the differences between the ALL and VLRF conditions observed in this study. Finally, we did not quantify the patella translation on the pressure-sensitive film in this study. However, we have previously shown that patella tracking in the rabbit PFJ is greatly affected by the knee extensor force and by anterior cruciate ligament transection, but not by VM weakness.35 VM weakness caused neither an appreciable medial-lateral translation nor a rotation of the patella in the frontal plane.35 Combining these findings with the results of our study, it suggests that VM weakness in the rabbit knee does not cause a shift in the PFJ contact area, but produces a vast increase in peak pressures with changes in the PFJ contact areas. Therefore, we are confident that changes in pressure distributions are not caused by linear translation of the patella relative to the femur, but rather, are associated with subtle 3-dimensional rotations of the patella.

An advantage of the current study compared with previous studies in this area is that we could control the individual muscles of the quadriceps group independently of each other and that the lines of actions of the muscles did not need to be estimated, as the entire knee joint/quadriceps system was left fully intact. This approach is highly versatile and can be used to study other aspects of PFJ mechanics, and it corrects the errors that have been made in human cadaveric studies where lines of actions of muscles were represented (incorrectly) by wires pulling along the distal muscle fiber direction.

We conclude from the results of this study that VM loss in the rabbit knee is associated with an increase in peak pressures and decrease in PFJ contact areas. These findings contradict previous results on the effects of VM weakness on rabbit PFJ mechanics, likely because of methodological differences between the studies. Our results support clinical and anecdotal evidence in human studies, where quadriceps weakness and strength imbalance have been associated with altered PFJ mechanics and patellofemoral pain. Since muscle weakness/imbalance has been shown to produce degeneration of the rabbit knee in as little as 4 weeks, we propose that quadriceps strength and balance are important factors in PFJ mechanics and patellofemoral pain.

Acknowledgments

This research is supported by the Canadian Institutes for Health Research (10013332); Canada Research Chair Program (RT730101); The Killam Foundation (10001203); Dean’s Doctoral Studentship in Kinesiology, University of Calgary; Eyes High International Doctoral Studentship, University of Calgary; and CONNECT! NSERC CREATE Program. The authors have no conflict of interest to disclose.

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    Elias JJ, Kilambi S, Cosgarea AJ. Computational assessment of the influence of vastus medialis obliquus function on patellofemoral pressures: model evaluation. J Biomech. 2010;43(4):612617. PubMed ID: 20060526 doi:10.1016/j.jbiomech.2009.10.039

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    Sawatsky A, Bourne D, Horisberger M, Jinha A, Herzog W. Changes in patellofemoral joint contact pressures caused by vastus medialis muscle weakness. Clin Biomech. 2012;27(6):595601. doi:10.1016/j.clinbiomech.2011.12.011

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    Maas H, Sandercock TG. Force transmission between synergistic skeletal muscles through connective tissue linkages. J Biomed Biotechnol. 2010;2010:575672. PubMed ID: 20396618 doi:10.1155/2010/575672.

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    Han SW, Sawatsky A, de Brito Fontana H, Herzog W. Contribution of individual quadriceps muscles to knee joint mechanics. J Exp Biol. 2019;222(6):jeb188292. PubMed ID: 30846537 doi:10.1242/jeb.188292

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    Ronsky JL, Herzog W, Brown TD, Pedersen DR, Grood ES, Butler DL. In vivo quantification of the cat patellofemoral joint contact stresses and areas. J Biomech. 1995;28(8):977983. PubMed ID: 7673264 doi:10.1016/0021-9290(94)00153-U

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    Leumann A, Fortuna R, Leonard T, Valderrabano V, Herzog W. Tibiofemoral loss of contact area but no changes in peak pressures after meniscectomy in a Lapine in vivo quadriceps force transfer model. Knee Surg Sports Traumatol Arthrosc. 2015;23(1):6573. PubMed ID: 25274087 doi:10.1007/s00167-014-3338-1

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    Egloff C, Sawatsky A, Leonard T, Fung T, Valderrabano V, Herzog W. Alterations in patellofemoral kinematics following vastus medialis transection in the anterior cruciate ligament deficient rabbit knee. Clin Biomech. 2014;29(5):577582. doi:10.1016/j.clinbiomech.2014.03.001

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    Clark AL, Herzog W, Leonard TR. Contact area and pressure distribution in the feline patellofemoral joint under physiologically meaningful loading conditions. J Biomech. 2002;35(1):5360. PubMed ID: 11747883 doi:10.1016/S0021-9290(01)00165-8

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    Rehan Youssef A, Longino D, Seerattan R, Leonard T, Herzog W. Muscle weakness causes joint degeneration in rabbits. Osteoarthritis Cartilage. 2009;17(9):12281235. doi:10.1016/j.joca.2009.03.017

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    Egloff C, Sawatsky A, Leonard T, Hart DA, Valderrabano V, Herzog W. Effect of muscle weakness and joint inflammation on the onset and progression of osteoarthritis in the rabbit knee. Osteoarthritis Cartilage. 2014;22(11):18861893. PubMed ID: 25106675 doi:10.1016/j.joca.2014.07.026

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    Roos EM, Herzog W, Block JA, Bennell KL. Muscle weakness, afferent sensory dysfunction and exercise in knee osteoarthritis. Nat Rev Rheumatol. 2011;7(1):5763. PubMed ID: 21119605 doi:10.1038/nrrheum.2010.195

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    Hinman RS, Lentzos J, Vicenzino B, Crossley KM. Is patellofemoral osteoarthritis common in middle-aged people with chronic patellofemoral pain? Arthritis Care Res. 2014;66(8):12521257. doi:10.1002/acr.22274

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    Segal NA, Torner JC, Felson D, et al. Effect of thigh strength on incident radiographic and symptomatic knee osteoarthritis in a longitudinal cohort. Arthritis Rheum. 2009;61(9):12101217. PubMed ID: 19714608 doi:10.1002/art.24541

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    Oiestad BE, Juhl CB, Eitzen I, Thorlund JB. Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis. Osteoarthritis Cartilage. 2015;23(2):171177. PubMed ID: 25450853 doi:10.1016/j.joca.2014.10.008

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    Maas H, Sandercock TG. Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat. J Appl Physiol. 2008;104(6):15571567. PubMed ID: 18339889 doi:10.1152/japplphysiol.01208.2007

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    Huijing PA. Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc Sport Sci Rev. 2003;31(4):167175. PubMed ID: 14571955 doi:10.1097/00003677-200310000-00003

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    Ward SR, Terk MR, Powers CM. Patella alta: association with patellofemoral alignment and changes in contact area during weight-bearing. J Bone Joint Surg Am. 2007;89(8):17491755. PubMed ID: 17671014 doi:10.2106/JBJS.F.00508

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    Sakai N, Luo ZP, Rand JA, An KN. The influence of weakness in the vastus medialis oblique muscle on the patellofemoral joint: an in vitro biomechanical study. Clin Biomech. 2000;15(5):335339. doi:10.1016/S0268-0033(99)00089-3

    • Crossref
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  • 49.

    Draper CE, Besier TF, Fredericson M, et al. Differences in patellofemoral kinematics between weight-bearing and non-weight-bearing conditions in patients with patellofemoral pain. J Orthop Res. 2011;29(3):312317. PubMed ID: 20949442 doi:10.1002/jor.21253

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    Wu JZ, Herzog W, Epstein M. Effects of inserting a pressensor film into articular joints on the actual contact mechanics. J Biomech Eng. 1998;120(5):655659. PubMed ID: 10412445 doi:10.1115/1.2834758

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Han, Sawatsky, Jinha, and Herzog are with the Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada. Herzog is also with the Biomechanics Laboratory, School of Sports, Federal University of Santa Catarina, Florianopolis, Santa Catarina, Brazil.

Han (seongwon.han@ucalgary.ca) is corresponding author.
  • View in gallery

    —Peak pressures (A) and contact areas (B) for the ALL and VLRF conditions. Peak pressures were greater and joint contact areas were smaller for the VLRF compared with the ALL condition. Open circles represent individual data points, and corresponding force matched pairs are connected by a thin dashed line. The short, horizontal bars indicate the mean values for each condition, and the long, vertical bars show ±1 SD from the mean. ALL indicates vastus lateralis (VL), vastus medialis, and rectus femoris (RF) were stimulated simultaneously; VLRF, only the VL and RF were stimulated simultaneously. Asterisks indicate statistical difference between the ALL and VLRF conditions (P < .05).

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    Stephen J, Alva A, Lumpaopong P, Williams A, Amis AA. A cadaveric model to evaluate the effect of unloading the medial quadriceps on patellar tracking and patellofemoral joint pressure and stability. J Exp Orthop. 2018;5(1):34. PubMed ID: 30203221 doi:10.1186/s40634-018-0150-8

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    Elias JJ, Kilambi S, Cosgarea AJ. Computational assessment of the influence of vastus medialis obliquus function on patellofemoral pressures: model evaluation. J Biomech. 2010;43(4):612617. PubMed ID: 20060526 doi:10.1016/j.jbiomech.2009.10.039

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    Sawatsky A, Bourne D, Horisberger M, Jinha A, Herzog W. Changes in patellofemoral joint contact pressures caused by vastus medialis muscle weakness. Clin Biomech. 2012;27(6):595601. doi:10.1016/j.clinbiomech.2011.12.011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Maas H, Sandercock TG. Force transmission between synergistic skeletal muscles through connective tissue linkages. J Biomed Biotechnol. 2010;2010:575672. PubMed ID: 20396618 doi:10.1155/2010/575672.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Han SW, Sawatsky A, de Brito Fontana H, Herzog W. Contribution of individual quadriceps muscles to knee joint mechanics. J Exp Biol. 2019;222(6):jeb188292. PubMed ID: 30846537 doi:10.1242/jeb.188292

    • Crossref
    • PubMed
    • Search Google Scholar
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  • 33.

    Ronsky JL, Herzog W, Brown TD, Pedersen DR, Grood ES, Butler DL. In vivo quantification of the cat patellofemoral joint contact stresses and areas. J Biomech. 1995;28(8):977983. PubMed ID: 7673264 doi:10.1016/0021-9290(94)00153-U

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Leumann A, Fortuna R, Leonard T, Valderrabano V, Herzog W. Tibiofemoral loss of contact area but no changes in peak pressures after meniscectomy in a Lapine in vivo quadriceps force transfer model. Knee Surg Sports Traumatol Arthrosc. 2015;23(1):6573. PubMed ID: 25274087 doi:10.1007/s00167-014-3338-1

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Egloff C, Sawatsky A, Leonard T, Fung T, Valderrabano V, Herzog W. Alterations in patellofemoral kinematics following vastus medialis transection in the anterior cruciate ligament deficient rabbit knee. Clin Biomech. 2014;29(5):577582. doi:10.1016/j.clinbiomech.2014.03.001

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Clark AL, Herzog W, Leonard TR. Contact area and pressure distribution in the feline patellofemoral joint under physiologically meaningful loading conditions. J Biomech. 2002;35(1):5360. PubMed ID: 11747883 doi:10.1016/S0021-9290(01)00165-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Rehan Youssef A, Longino D, Seerattan R, Leonard T, Herzog W. Muscle weakness causes joint degeneration in rabbits. Osteoarthritis Cartilage. 2009;17(9):12281235. doi:10.1016/j.joca.2009.03.017

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Egloff C, Sawatsky A, Leonard T, Hart DA, Valderrabano V, Herzog W. Effect of muscle weakness and joint inflammation on the onset and progression of osteoarthritis in the rabbit knee. Osteoarthritis Cartilage. 2014;22(11):18861893. PubMed ID: 25106675 doi:10.1016/j.joca.2014.07.026

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Roos EM, Herzog W, Block JA, Bennell KL. Muscle weakness, afferent sensory dysfunction and exercise in knee osteoarthritis. Nat Rev Rheumatol. 2011;7(1):5763. PubMed ID: 21119605 doi:10.1038/nrrheum.2010.195

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Slemenda C, Brandt KD, Heilman DK, et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med. 1997;127(2):97104. PubMed ID: 9230035 doi:10.7326/0003-4819-127-2-199707150-00001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Hinman RS, Lentzos J, Vicenzino B, Crossley KM. Is patellofemoral osteoarthritis common in middle-aged people with chronic patellofemoral pain? Arthritis Care Res. 2014;66(8):12521257. doi:10.1002/acr.22274

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Segal NA, Torner JC, Felson D, et al. Effect of thigh strength on incident radiographic and symptomatic knee osteoarthritis in a longitudinal cohort. Arthritis Rheum. 2009;61(9):12101217. PubMed ID: 19714608 doi:10.1002/art.24541

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Kulig K, Andrews JG, Hay JG. Human strength curves. Exerc Sport Sci Rev. 1984;12(1):417466. PubMed ID: 6376139 doi:10.1249/00003677-198401000-00014

  • 44.

    Oiestad BE, Juhl CB, Eitzen I, Thorlund JB. Knee extensor muscle weakness is a risk factor for development of knee osteoarthritis. A systematic review and meta-analysis. Osteoarthritis Cartilage. 2015;23(2):171177. PubMed ID: 25450853 doi:10.1016/j.joca.2014.10.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Maas H, Sandercock TG. Are skeletal muscles independent actuators? Force transmission from soleus muscle in the cat. J Appl Physiol. 2008;104(6):15571567. PubMed ID: 18339889 doi:10.1152/japplphysiol.01208.2007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Huijing PA. Muscular force transmission necessitates a multilevel integrative approach to the analysis of function of skeletal muscle. Exerc Sport Sci Rev. 2003;31(4):167175. PubMed ID: 14571955 doi:10.1097/00003677-200310000-00003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    Ward SR, Terk MR, Powers CM. Patella alta: association with patellofemoral alignment and changes in contact area during weight-bearing. J Bone Joint Surg Am. 2007;89(8):17491755. PubMed ID: 17671014 doi:10.2106/JBJS.F.00508

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Sakai N, Luo ZP, Rand JA, An KN. The influence of weakness in the vastus medialis oblique muscle on the patellofemoral joint: an in vitro biomechanical study. Clin Biomech. 2000;15(5):335339. doi:10.1016/S0268-0033(99)00089-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 49.

    Draper CE, Besier TF, Fredericson M, et al. Differences in patellofemoral kinematics between weight-bearing and non-weight-bearing conditions in patients with patellofemoral pain. J Orthop Res. 2011;29(3):312317. PubMed ID: 20949442 doi:10.1002/jor.21253

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Wu JZ, Herzog W, Epstein M. Effects of inserting a pressensor film into articular joints on the actual contact mechanics. J Biomech Eng. 1998;120(5):655659. PubMed ID: 10412445 doi:10.1115/1.2834758

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
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