University of Groningen

Motor control after anterior cruciate ligament reconstructionGokeler, Alli

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UITNODIGING

voor het bijwonen van de openbare verdediging

van mijn proefschrijft

Motor Control after

Anterior Cruciate Ligament Reconstruction

op woensdag 11 maart om 16:15 uur

Academiegebouw van de Rijksuniversiteit Groningen Broerstraat 5 te Groningen

Na afloop bent u van harte welkom op de receptie in

het Academiegebouw.

Alli Gokeler

Paranimfen Wouter Welling Malou Alferink

allipromotie@gmail.com

Motor Control after A

nterior Cruciate Ligament Reconstruction

Alli Gokeler

Motor Control after

Anterior Cruciate Ligament Reconstruction

Alli Gokeler

Gokeler_Omslag.indd 1 16-02-15 09:06

Motor Control after Anterior CruciateLigament Reconstruction

Alli Gokeler

Alli GokelerMotor Control after Anterior Cruciate Ligament ReconstructionDissertation University of Groningen, The Netherlands. With summary in Dutch.

ISBN: 978-94-91487-21-7

Cover by: Edwin Keijzer (www.edwinkeijzer.nl) Layout by: Nikki Vermeulen, Ridderprint BV, Ridderkerk, the NetherlandsPrinted by: Ridderprint BV, Ridderkerk, the NetherlandsPublisher: Medix Publishers BV, Keizersgracht 317A, 1016 EE Amsterdam, the Netherlands

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The photographs in this dissertation are courtesy of Edwin Keijzer (www.edwinkeijzer.nl)and photograph cover chapter 5 courtesy of Bert Otten (http//:www.photoplaza.nl/lindolfi)

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Motor Control after Anterior CruciateLigament Reconstruction

Proefschrift

ter verkrijging van de graad van doctor aan de Rijksuniversiteit Groningen

op gezag van de rector magnificus prof. dr. E. Sterken

en volgens besluit van het College voor Promoties.

De openbare verdediging zal plaatsvinden op

woensdag 11 maart 2015 om 16:15 uur

door

Alouis Gokeler

geboren op 18 september 1967te Groningen

Promotores Prof. dr. E.Otten Prof. dr. K. Postema Prof. dr. P.U. Dijkstra

Co-promotor Dr. M.P. Arnold

Beoordelingscommissie Prof. dr. R.L. Diercks Prof. dr. L.H.V. van der Woude Prof. dr. J. Duysens

TA B L E O F C O N T E N T S

Chapter 1 Introduction 7

Chapter 2 The Relationship between Isokinetic Quadriceps Strength and 13 Laxity on Gait Analysis Parameters in ACL Reconstructed Knees.

Chapter 3 Abnormal Landing Strategies after ACL Reconstruction. 27

Chapter 4 Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant? 43 A Systematic Review.

Chapter 5 Movement Patterns of Patients Immersed in Virtual Reality 71 after ACL Reconstruction.

Chapter 6 Summary 85

Chapter 7 General Discussion 99

Acknowledgment 111 About the Author 117 Financial Support 127

Chapter 1Introduction

Introduction

Chapter

1

9

I N T R O D U C T I O N

Of all athletic knee injuries, a rupture of the anterior cruciate ligament (ACL) is most common and most devastating, resulting in the greatest time lost from sport participation.1 The ACL plays a vital role in the normal function and stability of the knee. Specifically, the native ACL consists of an anteromedial (AM) and posterolateral (PL) bundle, which together provide anterior and rotational stability of the knee.2 Due to its inherent contributions to joint stability and function, when injured, it is widely accepted in the orthopedic community that treatment of choice for an active person should be surgical reconstruction.3

However, successful ACL-reconstruction (ACLR) in terms of restoring the mechanical stability of the knee joint does not ensure restoration of normal knee function. Moreover, despite the fact that surgical techniques and rehabilitation have evolved over the last decade, there is an ongoing debate related to the long term outcome of surgical versus a non-surgical approach.4 An ACL injury increases the risk of osteoarthritis (OA) and until now, ACLR has not been able to revert that course. Altered movement patterns after ACLR have been linked to early development of OA. It has been shown that for months and even years after ACLR, deficits in common daily activities as gait as well as athletic activities such as running and jumping and landing exist. The aim of this dissertation is to contribute to the body of knowledge that may help us to understand the causes of altered movement patterns after ACLR.

O U T L I N E O F T H E D I S S E R TAT I O N

Chapter 2In chapter 2, the results of gait analysis conducted six months after ACLR are presented. In this study the relationships between frequent clinical outcome measurements such as strength and anterior laxity of the knee and gait parameters were determined. Previous studies reported on altered gait after ACLR but were more or less descriptive in nature. This study was undertaken to aid in our understanding as to why patients demonstrate altered gait patterns after ACLR. We chose the six months time frame to study these measures as it is common to release patients to sports after this period of rehabilitation.

Chapter 3In one of our previous studies we determined that gait had returned to normal levels in only about a third of all patients at one year after ACLR.5 Gait can be considered an activity with relative low intensity and as most patients after ACLR desire to return to

Chapter 1

10

high demanding activities, we were therefore interested in examining more demanding tasks in chapter 3. In the final stages of rehabilitation, hop test are commonly used to determine if patients after ACLR can return to sports. Thus, if hop tests are used as indicators of the functional performance after ACLR, it is imperative that a comprehensive assessment is carried out that includes a kinematic, kinetic and EMG-analysis. In this study, such a comprehensive examination was conducted in order to better understand the biomechanical and neuromuscular profiles at the time of release to sports.

Chapter 4The first two experiments presented in this dissertation provided descriptive information related to altered function following ACLR. Additional proposed mechanisms are related to altered proprioception after ACL injury.6 The ACL contains mechanoreceptors which relay proprioceptive information to the central nervous system (CNS), which may activate the muscles around the knee for stabilization. However the precise mechanism is subject of controversy. In this chapter a literature review was conducted with the specific aim to find relationships between proprioception and often used clinical outcome measures as muscle strength, laxity, hop test, balance and patient-reported outcome.

Chapter 5The two biomechanical studies that are presented in this dissertation, offer only descriptions of the changed movement patterns after ACLR. However they fail to provide an explanation of the phenomena encountered. In chapter 5, a new theoretical framework to fill this gap is presented. The contention is that patients after ACLR may utilize an increased attentional, cognitive focus on movements which inhibits the learning process to regain normal movements. We employed virtual reality as a tool to explore the effect of cognitive motor control during an easy and common daily task.

Chapters 6 and 7In chapters 6 and 7, the findings of the research projects are summarized and placed in perspective with an outline for future research.More specifically, thought-provoking issues are presented pertaining the potential causes of altered movements as well a paradigm change in terms of rehabilitation.

Introduction

Chapter

1

11

R E F E R E N C E S1. Dick R, Hootman JM, Agel J, Vela L, Marshall SW, Messina R. Descriptive epidemiology of collegiate

women’s field hockey injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2002-2003. J Athl Train. 2007;42(2):211-220.

2. van Eck CF, Kopf S, Irrgang JJ, et al. Single-bundle versus double-bundle reconstruction for anterior cruciate ligament rupture: a meta-analysis--does anatomy matter? Arthroscopy. 2012;28(3):405-424.

3. Marx RG, Jones EC, Angel M, Wickiewicz TL, Warren RF. Beliefs and attitudes of members of the American Academy of Orthopaedic Surgeons regarding the treatment of anterior cruciate ligament injury. Arthroscopy. 2003;19(7):762-770.

4. Delince P, Ghafil D. Anterior cruciate ligament tears: conservative or surgical treatment? A critical review of the literature. Knee Surg Sports Traumatol Arthrosc. 2012;20(1):48-61.

5. Schmalz T, Blumentritt S, Wagner R, Gokeler A. Gait analysis of patients within one year after anterior cruciate ligament reconstruction. Phys Med Reh Kurortmed. 1998;8:1-8.

6. Friden T, Roberts D, Ageberg E, Walden M, Zatterstrom R. Review of knee proprioception and the relation to extremity function after an anterior cruciate ligament rupture. J Orthop Sports Phys Ther. 2001;31(10):567-576.

Chapter 2The Relationship between Isokinetic Quadriceps Strength and Laxity on Gait Analysis Parametersin ACL Reconstructed Knees

A. Gokeler, T. Schmalz, E. Knopf, J. Freiwald, S. BlumentrittKnee Surg Sports Traumatol Arthrosc 2003; 11(6):372–378

Chapter 2

14

A B S T R A C T

Gait alterations after anterior cruciate ligament (ACL) reconstruction have been reported in the literature. In the current study, a group of 14 patients who all had an ACL-reconstruction (ACLR) with a patellar tendon autograft were examined. Kinetic and kinematic data were obtained from the knee during walking. The Flexion-Extension-Deficit (FED) calculated from the angular difference between maximal flexion and maximal extension during the stance phase in the ACLR and the normal knee was measured. We investigated whether these alterations in gait are related to quadriceps strength and residual laxity of the knee. It may be that patients modify their gait patterns to protect the knee from excessive anterior translation of the tibia by reducing the amount of extension during stance. On the other hand, persistent quadriceps weakness may also cause changes in gait patterns as the quadriceps is functioning as an important dynamic stabilizer of the knee during stance. Results showed that patients had a significantly higher FED value of 4.9 ± 4.0 when compared to data obtained from a healthy control group (CTRL) in a previous stud (FED 1.3 ± 0.9). This is mainly caused by an extension deficit during mid stance. External extension moments of the knee were significantly lower in the ACLR group -0.27 ± 0.19 TZMAX Nm/kg when compared to a CTRL group -0.08 ± 0.06 TZMAX Nm/kg. Correlation coefficient analysis did not show any positive relationship between quadriceps strength and gait analysis parameters. Furthermore no correlation was found between the amount of laxity of the knee and gait. The relevance of this study lies in the fact that apparently the measured gait alterations cannot be solely explained by often used biomechanical indicators such as laxity and strength. Possibly, the measured gait alterations are a result of the surgical procedure with subsequent modified motor programming.

Key words: ACL, Gait analysis, Isokinetic strength, Neuromuscular, Rehabilitation

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15

I N T R O D U C T I O N

Anterior cruciate ligament-reconstruction (ACLR) has become a routine surgical procedure in the last 15 years. Since the early nineties more aggressive rehabilitation programs have been advocated including immediate full knee extension, weight bearing as tolerated and early initiation of closed chain exercises emphasizing quadriceps strengthening.1 Subsequently coordinative exercises are implemented with the goal of return to sports at four-six months after surgery. Several quantitative tests are described in the literature such as arthrometric knee laxity testing1-3 and isokinetic strength testing4-6 to evaluate the outcome of these surgical procedures. It has been demonstrated that laxity tests may not necessarily provide information about the functional status of the knee.7 Furthermore, it is commonly accepted that return of a strong quadriceps muscle after knee injuries is vital for functional and athletic use of the lower extremity8-11 although others did not observe this correlation.12,13 Reports about isokinetic peak torque measurements taken approximately six months after ACLR and comparing the involved with the non-involved side show quadriceps ratios ranging from 59.5% to more then 90%.5,6,14-17 Despite the differences reported, the consensus seems that quadriceps strength has not returned to normal levels at this time after surgery. This is interesting considering that most athletes are able to resume sports approximately six months after surgery. We know from investigations performed at our gait laboratory18 that a large percentage of patients show significant abnormalities during gait even at 26 weeks after ACLR, equivalent to the time period when most patients return to sports. In fact, the evidence from our study showed that the return of normal gait may even take more than one year. The most striking differences were an extension deficit and reduced external extension moments in the involved knee in the mid-stance phase of gait. The question arises as to the nature of different biomechanical strategies used – consciously or unconsciously - by patients after ACLR. It may be that patients modify their gait patterns to protect the knee from excessive anterior translation of the tibia by reducing the amount of extension during stance. On the other hand persistent quadriceps weakness may also cause changes in gait patterns as the quadriceps is functioning as an important dynamic stabilizer of the knee during stance. The purpose of this study was to determine whether gait alterations were present in patients whose ACL-deficient (ACLD) knees were surgically reconstructed with a patellar tendon autograft, and in that case, whether that had a relationship with residual laxity and quadriceps strength. We chose to take the measurements 26 weeks after surgery as we know from a previous study that kinetic and kinematic characteristics of gait are still significantly different from controls.19

Chapter 2

16

M AT E R I A L A N D M E T H O D S

SubjectsFourteen subjects (7 men and 7 women) with a mean age of 24 years (range 21-40),mean height 183 cm (range 162-192) and a mean weight of 74.4 kg (range 56-101) participated in this study. All had a complete rupture of the ACL that was arthroscopically reconstructed using the central third of the patellar tendon. All patients participating in the study were collegiate or recreational athletes. After surgery, they completed an intensive rehabilitation program as outpatients three times a week at the same rehabilitation center. The program included immediate weight bearing, range of motion exercises, pool therapy, stationary bicycle and closed chain strengthening and coordination exercises. Running was permitted after 10 weeks and once dynamic stability was satisfactory, agility and sports specific exercises were started. Return to sports involving pivoting and jumping was allowed after six months. Patients gave their consent to participate in this study.

Experimental DesignClinical examinationAll patients were examined by the same two physical therapists with respectively ten and eight years experience in orthopedics. The examination consisted of passive range of motion measurements of both knees for knee extension and flexion with a standard goniometer and instrumented laxity testing using the KT-1000 arthrometer (MEDmetric Corp., San Diego, Cal. USA) tests with application of a 89-N force. Side-to-side differences (in mm) were reported for comparison.

Isokinetic testingMuscular performance of both knees was evaluated on an isokinetic testing device (Lido Active, Loredon Biomedical Inc., Davis, CA) of both knees at a velocity of 60 deg/sec. All patients had two-three training sessions on the isokinetic device in the weeks prior to testing to familiarize them with the testing procedure. The subjects did a 15 minute warm-up on a stationary bicycle (Kardiomed Bike, Proxomed, Karlstein, Germany) before the test procedure. Testing was done with the subjects in a seated position with the hip in 90° flexion and the thigh fixated with straps. The ROM for the knee was set at 0° to 90° flexion. The noninvolved side was tested first. Prior to testing 10 sub-maximal repetitions were performed. The test procedure consisted of 10 maximal concentric repetitions for flexion and extension at a speed of 60 deg/sec. The patients received standardized verbal commands but visual information from the curves as displaced on the monitor was withheld. The peak torque of quadriceps and hamstring strength was

The Relationship between Isokinetic Quadriceps Strength and Laxity

Chapter

2

17

compared with the noninvolved side and was expressed as a ratio (involved torque/noninvolved torque x 100).

Gait analysisGait analysis was performed for level walking at our gait laboratory using a 4-camera optoelectric system (Primas, Delft Motion Analysis, Delft, the Netherlands) with a 100 Hz frequency for collection of the 2-dimensional data. Reflective markers were placed on the subjects at anatomic landmarks according to the description in a previous paper.18 The markers were placed at the greater trochanter, lateral femoral epicondyle, lateral malleolus and on the outside of the shoe representing the location of the head of the fifth metatarsal. Thus only sagittal plane motions could be calculated. Two force plates (Kistler Instruments, Winterthur, Switzerland) embedded in a 12 meter long walkway measured the ground reaction forces of both legs with a sampling rate of 400 Hz. The 2-dimensional data derived from the four cameras were synchronized with the collection of data from the force plates. All subjects were instructed to walk steadily during the test procedure. For each subject a specific starting point was determined from test trials so that the subject would contact the platform each time with the same limb without having to consciously focus to touch the plate. All subjects walked with sport shoes. The data used in this study were obtained from the mean values of 10-12 consistent cycles of walking over the walkway. Definitions of the quantitative parameters were described in detail in an earlier publication from our institution.18 For the purpose of this study we will summarize the most important kinetic and kinematic parameters. To describe the kinematic changes during the stance phase, we calculated the angular difference between maximal flexion and maximal extension in the ACLR and the normal knee. We defined this as the “Flexion-Extension-Deficit“ (FED) (Figure 1). The differentiation whether a significant FED-value is due to reduced flexion or extension motion during stance can be made with the calculation of joint toques. In 90% of the cases a higher value is associated with an extension deficit in stance.18

D ACL D NOR

θ [°] θ [°] 180 180

140 140 20 60 20 60 t [%] t [%]

FED = D ACL - D NOR

Figure 1. Sagittal knee angles (θ) during the stance phase (t expressed as percentage of stance phase) for the reconstructed knee (left) and normal knee (right). DACL Difference between maximal knee flexion an extension for the reconstructed knee; DNOR difference between maximal knee flexion an extension for the normal knee; FED DACL–DNOR

Chapter 2

18

The external, sagittal moment acting on the knee joint was calculated from kinematic data and ground reaction forces. During normal human gait there is an external flexion moment in the first 50% of stance which is followed by an external extension moment in the second half. The difference between the maximal values of the external flexion moments comparing the ACLR knee with the normal knee is defined as TZMIN whereas the difference between maximal external extension moments is defined as TZMAX (Figure 2).

Figure 2. The sagittal knee moments during stance phase (t expressed as percentage of stance phase) normalized to body weight (MZ). The external flexion (MZMIN) and extension (MZMAX) moments are shown for the ACL-reconstructed knee (left) and normal knee (right). The difference between the maximal values of the external flexion moments comparing the ACL-reconstructed knee with the normal knee is defined as TZMIN

whereas the difference between maximal external extension moments is defined as TZMAX.

In this study we only calculated for TZMAX as this was shown to be a sensitive indicator of gait abnormalities.18 All measurements were performed 26 weeks after surgery on all subjects.

Statistical analysisLinear correlation coefficients were calculated with SPSS 10.0 for Windows to determine the relationship between isokinetic strength, laxity measurements and gait analysis.

R E S U LT S

Gait analysisThe mean value of FED in our patients during stance phase of gait was 4.9° ± 4.0 and was significantly different (p < 0.01) when compared to a control group in a previous study. (Figure 3). The mean external extension torque, TZMAX was - 0.27 ± 0.19 Nm/kg and is also significantly different (p < 0.05) when compared to controls (Figure 4).

The Relationship between Isokinetic Quadriceps Strength and Laxity

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FED

[º]

0

1.5

3

4.5

6

Patients current study Patients previous study Controls

Figure 3. Kinematic flexion extension deficit FED for the current patient group in comparison to the earlier recorded data of a comparable patient group (n=35, mean age 27 years) and a healthy control group (n=30, mean age 28 years)28 indicating significant difference (*) of the patients in comparison to the natural right-left-differences of uninjured people (p < 0.01).

Tzm

ax [

Nm

/kg

]

0

0.1

0.2

0.3

0.4

Patients current study Patients previous study Controls

Figure 4. External extension moments TZMAX for the current patient group in comparison to the earlier recorded data of comparable patient group (n=35, mean age 27 years) and a healthy control group (n=30, mean age 28 years)28 indicating significant difference (*) of the patients in comparison to the natural right-left-differences of uninjured people (p < 0.05).

Laxity examination and Isokinetic StrengthLaxity measurements with the KT-1000 with a 89N force showed a mean side to side difference of 2 ± 0.9 mm. The mean isokinetic quadriceps peak torque ratio at 60 deg/sec for the involved side was 74.9 ± 17.8 % of the non-involved side.

*

*

*

*

Chapter 2

20

Correlation between Laxity, Isokinetic Strength and Gait AnalysisThe linear correlation coefficients between clinical examination, isokinetic strength and gait analysis were calculated and are summarized in Table 1. A correlation exists between FED and TZMAX (p < 0.05). We did not find a correlation between laxity examination, isokinetic quadriceps torque and gait analysis parameters.

Table 1. Correlation coefficients (r) between the Gait Analysis Parameters FED and TZMAX and Isokinetic Quadriceps Peak Torque and Laxity

TZMAX KT-1000 Isokinetic Quadriceps Peak Torque

FED 0.56 (*) 0.005 0.33

TZMAX X 0.19 0.24

(*: indicates statistically significant relationship p<=0.05)

We present 4 scatter diagrams: one showing the correlation between FED and isokinetic quadriceps peak torque (Figure 5), one showing the correlation between TZMAX and laxity (Figure 6), one showing the correlation between FED and laxity (Figure 7) and finally between TZMAX and isokinetic quadriceps strength (Figure 8).

Figure 5. Correlation between the kinematic Flexion-Extension Deficit (FED) and Isokinetic Quadriceps Peak Torque in ACL-reconstructed knees.

[Nm

]

The Relationship between Isokinetic Quadriceps Strength and Laxity

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Figure 6. Correlation between TZMAX and Laxity in ACL-reconstructed knees.

Figure 7. Correlation between FED and Laxity in ACL-reconstructed knees.

Figure 8. Correlation between TZMAX and Isokinetic Quadriceps Peak Torque in ACL-reconstructed knees.

[Nm

]

Chapter 2

22

D I S C U S S I O N

The results from this study showed that typical kinetic and kinematic deficits are present after ACLR. The abnormalities mainly concern ROM, the extension motion of the knee, and the external extension moments acting on the knee joint during the stance phase of gait. In this context a statistical relationship exists between FED and TZMAX. In other words, we found that when FED reaches normal values it will implicate that the most important kinetic parameter expressed as TZMAX , will have also returned to normal values.18 Neither FED nor TZMAX were related to quadriceps strength or laxity of the knee. The concept of gait modification in ACLD knees termed quadriceps avoidance as a strategy to reduce anterior displacement of the tibia is perhaps the one most popularized.20,21 Others did not demonstrate the phenomenon of quadriceps avoidance.18,19,22-24 Cicotti et al.25 reported consistent EMG activity of the vastus lateralis muscle during gait in patients with ACLD knees when compared to controls. Our results concerning the absence of a significant relationship between laxity and gait analysis are in general agreement with Rudolph and co-workers.26 They examined subjects with ACLD knees who were classified as copers and non-copers. The copers compensated well functionally for ACL injury compared to non-copers who were not able to stabilize their knees and were scheduled for surgery. They found that the amount of laxity in their subjects was unrelated to gait patterns. The aforementioned contradictions in the literature may be due to differences in methodology by which kinetic and kinematic data are calculated, examination of ACLD or ACLR knees, time after surgery, sample size and statistical analysis used. Our study showed that six months after ACLR, patients had a mean isokinetic quadriceps peak torque ratio of 74.9% which is in proximity of values reported by others.6,14,17 Our results showed no statistical relationships between isokinetic quadriceps strength and gait analysis parameters. Some researchers have found positive relationships between isokinetic quadriceps peak torque and functional performance8,9,11 others found only a low or no correlation.12,13,27,28 Several papers examining the effect of strength on gait analysis have been published. Snyder-Mackler and co-workers10 studied 110 patients after ACLR and showed a relationship between isometric quadriceps strength and lower values of extension and flexion motion during the stance phase. In general the kinematic differences they reported are in agreement with our study, however in contrast to their findings, the differences we measured were unrelated to quadriceps strength. Lewek et al.29 examined the relationship between isometric strength of the quadriceps on gait mechanics. They classified patients with ACLR knees in two groups of strong quadriceps with strength ratios > 90% and those with ratios < 80%. They found a significant relationship between strength and knee angles and moments during the early phase of stance. Mittlmeier and colleagues30 found that weakness of the quadriceps

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measured isokinetically 24 weeks after ACLR was related to gait abnormalities. However they studied gait by assessing plantar pressure distribution which cannot calculate for joint moments as we did in our study. Rudolph et al.26 did not find a correlation between isometric quadriceps strength and the amount of knee flexion during weight acceptance in subjects with ACL-deficient knees. It has to be noted that isokinetic testing usually involves maximal muscle activation whereas kinetic and kinematic parameters obtained during gait do not place maximal demands on the knee joint. This could be a possible explanation for the lack of relationship between isokinetic quadriceps strength and gait analysis parameters. Several investigators22,23,31 have described the dynamic stabilizing function of the hamstrings in ACLD knees. Less is known about the role of the hamstrings in a population with ACLR knees. Cicotti and co-workers25 reported near normal activity of the hamstrings during the swing phase of gait in ACLR knees when compared to controls. Work at our own institution has shown that the activity of the gastrocnemius muscle is significantly reduced during the stance phase.32 Although improvements in surgical techniques and more aggressive rehabilitation programs have been implemented, several authors continue to report persistent deficits in quadriceps strength.33-35 Engelhardt and co-workers showed that afferent signals from the central nervous system inhibit the activation of the quadriceps muscle after injury or surgery of the knee, causing the often observed atrophy of the quadriceps.36 Freiwald and colleagues demonstrated that isokinetic torque of the quadriceps was significantly reduced 12 weeks after ACLR when compared to pre-operative measurements.33,37 At 16 months after surgery the maximal isokinetic quadriceps ratio was 81% in comparison to the normal knee. Interestingly the patients had a Lysholm score > 95 points and had all resumed their pre-operative sports level. Recently, Keays et al. corroborated these findings.6 They showed that an isokinetic peak torque ratio of the quadriceps of 88% before surgery and decreasing to 72% at six months after surgery despite intensive quadriceps training. Interestingly, functional tests improved by in the same time period. One may conclude that isokinetic quadriceps peak torque is not as important a predictor of function as initially thought. It may be that when a - so far undefined - “peak torque deficit” is crossed, subjective and objective limitations may become noticeable. From the perspective of the theories in motor learning it appears that reprogramming of the central nervous system after ACLR allows for improvement of functional tasks despite weakness of the quadriceps.38 The clinical implication may be that primarily focusing on return of full quadriceps strength is no longer warranted and rehabilitation should rather implement goal-oriented exercises that replicate the functional demands as in sports or work.38

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Several limitations have to be addressed about this paper. First, we had a relative small patient population. Second, the data derived can only be applied to patients who underwent the same surgical procedures as in our study population. Third, to the best of our knowledge, the external validity of gait analysis has has not been demonstrated to more athletic functional demands of the knee. The kinematic and kinetic data as measured in this study thus only applies to gait. Studying more strenuous activities such as running, jumping and cutting movements may provide more relevant information about the differences in kinetic and kinematic parameters necessary for sports related function of the knee. They could then be used as indicators of a safe return to sports after ACLR-reconstruction. Our study clearly indicates that gait analysis parameters in ACLR knees are not related to quadriceps strength and laxity. Central reprogramming of the central nervous system38 may be the reason why gait is significantly altered after surgical reconstruction of the ACL39 as these changes cannot be fully explained by quadriceps weakness and laxity of the knee.

AcknowledgmentsOtto Bock Research Department, Biomechanics Laboratory, Göttingen, Germany

Declaration We followed the principles outlined in the Declaration of Helsinki and the experiment complied with the law in Germany. The subjects were free to withdraw from the study at any time.

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R E F E R E N C E S1. Shelbourne KD, Nitz P. Accelerated rehabilitation after anterior cruciate ligament reconstruction. Am J

Sports Med. 1990;18(3):292-299.

2. Bach BR, Jr., Jones GT, Hager CA, Sweet FA, Luergans S. Arthrometric results of arthroscopically assisted anterior cruciate ligament reconstruction using autograft patellar tendon substitution. Am J Sports Med 1995;23(2):179-185.

3. Daniel DM, Malcom LL, Losse G, Stone ML, Sachs R, Burks R. Instrumented measurement of anterior laxity of the knee. J Bone Joint Surg Am. 1985;67(5):720-726.

4. Witvrouw E, Bellemans J, Verdonk R, Cambier D, Coorevits P, Almqvist F. Patellar tendon vs. doubled semitendinosus and gracilis tendon for anterior cruciate ligament reconstruction. Int.Orthop. 2001;25(5):308-311.

5. Carter TR, Edinger S. Isokinetic evaluation of anterior cruciate ligament reconstruction: hamstring versus patellar tendon. Arthroscopy. 1999;15(2):169-172.

6. Keays SL, Bullock-Saxton J, Keays AC. Strength and function before and after anterior cruciate ligament reconstruction. Clin Orthop Relat Res. 2000(373):174-183.

7. Snyder-Mackler L, Fitzgerald GK, Bartolozzi AR, 3rd, Ciccotti MG. The relationship between passive joint laxity and functional outcome after anterior cruciate ligament injury. Am J Sports Med. 1997;25(2):191-195.

8. Barber SD, Noyes FR, Mangine RE, McCloskey JW, Hartman W. Quantitative assessment of functional limitations in normal and anterior cruciate ligament-deficient knees. Clin Orthop Relat Res. 1990(255):204-214.

9. Noyes FR, Barber SD, Mangine RE. Abnormal lower limb symmetry determined by function hop tests after anterior cruciate ligament rupture. Am J Sports Med. 1991;19(5):513-518.

10. Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW. Strength of the quadriceps femoris muscle and functional recovery after reconstruction of the anterior cruciate ligament. A prospective, randomized clinical trial of electrical stimulation. J Bone Joint Surg Am. 1995;77(8):1166-1173.

11. Karlsson J, Kalebo P, Goksor LA, Thomee R, Sward L. Partial rupture of the patellar ligament. Am J Sports Med. 1992;20(4):390-395.

12. Anderson MA, Gieck JH, Perrin DH, Weltman A, Rutt RA, Denegar CR. The Relationships among Isometric, Isotonic, and Isokinetic Concentric and Eccentric Quadriceps and Hamstring Force and Three Components of Athletic Performance. J Orthop Sports Phys Ther. 1991;14(3):114-120.

13. Delitto A, Irrgang JJ, Harner CD, Fu FH. Relationship of Isokinetic Quadriceps Peak Torque and Work to One Legged Hop and Vertical Jump in ACL Reconstructed Knees. Phys Ther. 1993;73(6):S85.

14. Shelbourne KD, Foulk DA. Timing of surgery in acute anterior cruciate ligament tears on the return of quadriceps muscle strength after reconstruction using an autogenous patellar tendon graft. Am J Sports Med. 1995;23(6):686-689.

15. Wilk KE, Romaniello WT, Soscia SM, Arrigo CA, Andrews JR. The relationship between subjective knee scores, isokinetic testing, and functional testing in the ACL-reconstructed knee. J Orthop Sports Phys Ther. 1994;20(2):60-73.

16. Wilk KE, Keirns MA, Andrews JR, Clancy WG, Arrigo CA, Erber DJ. Anterior cruciate ligament reconstruction rehabilitation: a six-month followup of isokinetic testing in recreational athletes. Isokinet Exc Sci. 1991;1(1):36.

17. Wilk KE, Andrews JR. Current concepts in the treatment of anterior cruciate ligament disruption. J Orthop Sports Phys Ther. 1992;15(6):279-293.

18. Schmalz T, Blumentritt S, Wagner R, Gokeler A. Gait analysis of patients within one year after anterior cruciate ligament reconstruction. Phys Med Reh Kurortmed. 1998;8:1-8.

19. Schmalz T, Blumentritt S, Wagner R, Junge R. [Evaluation with biomechanical gait analysis of various treatment methods after rupture of the anterior cruciate ligament]. Sportverletz Sportschaden. 1998;12(4):131-137.

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20. Andriacchi TP, Birac D. Functional testing in the anterior cruciate ligament-deficient knee. Clin Orthop Relat Res. Mar 1993(288):40-47.

21. Berchuck M, Andriacchi TP, Bach BR, Reider B. Gait adaptations by patients who have a deficient anterior cruciate ligament. J Bone Joint Surg Am. 1990;72(6):871-877.

22. Beard DJ, Soundarapandian RS, O’Connor JJ, Dodd CA. Gait and electromyographic analysis of anterior cruciate ligament deficient subjects. Gait Posture. 1996;4(2):83.

23. Roberts CS, Rash GS, Honaker JT, Wachowiak MP, Shaw JC. A deficient anterior cruciate ligament does not lead to quadriceps avoidance gait. Gait Posture. 1999;10(3):189-199.

24. Timoney JM, Inman WS, Quesada PM, et al. Return of normal gait patterns after anterior cruciate ligament reconstruction. Am J Sports Med. 1993;21(6):887-889.

25. Ciccotti MG, Kerlan RK, Perry J, Pink M. An electromyographic analysis of the knee during functional activities. II. The anterior cruciate ligament-deficient and -reconstructed profiles. Am J Sports Med. 1994;22(5):651-658.

26. Rudolph KS, Eastlack ME, Axe MJ, Snyder-Mackler L. 1998 Basmajian Student Award Paper: Movement patterns after anterior cruciate ligament injury: a comparison of patients who compensate well for the injury and those who require operative stabilization. J Electromyogr Kinesiol. 1998;8(6):349-362.

27. Sekiya I, Muneta T, Ogiuchi T, Yagishita K, Yamamoto H. Significance of the single-legged hop test to the anterior cruciate ligament-reconstructed knee in relation to muscle strength and anterior laxity. Am J Sports Med. 1998;26(3):384-388.

28. Kovaleski JE, Heitman RJ, Andrew DP, Gurchiek LR, Pearsall AW. Relationship between closed-linear-kinetic- and open-kinetic-chain isokinetic strength and lower extremity functional performance. J Sport Reh. 2001;10(3):196.

29. Lewek M, Rudolph K, Axe M, Snyder-Mackler L. The effect of insufficient quadriceps strength on gait after anterior cruciate ligament reconstruction. Clin Biomech. 2002;17(1):56-63.

30. Mittlmeier T, Weiler A, Sohn T, et al. Functional monitoring during rehabilitation following anterior cruciate ligament reconstruction. A novel Award Second Prize Paper. Clin Biomech. 1999;14(8):576-584.

31. Liu W, Maitland ME. The effect of hamstring muscle compensation for anterior laxity in the ACL-deficient knee during gait. J Biomech. 2000;33(7):871-879.

32. Schmalz T, Freiwald J, Greiwing A, Kocker L, Ludwig H, Blumentritt S. Mechanical and electromyographical gait parameters in the course of rehabilitation after anterior cruciate ligament reconstruction. Eur J Sports Traumatol Relat Res 2001;23(4):146-151.

33. Freiwald J, Jager A, Starker M. [EMG-assisted functional analysis within the scope of follow-up of arthroscopically managed injuries of the anterior cruciate ligament]. Sportverletz Sportschaden. 1993;7(3):122-128.

34. Yasuda K, Ohkoshi Y, Tanabe Y, Kaneda K. Quantitative evaluation of knee instability and muscle strength after anterior cruciate ligament reconstruction using patellar and quadriceps tendon. Am J Sports Med. 1992;20(4):471-475.

35. Natri A, Jarvinen M, Latvala K, Kannus P. Isokinetic muscle performance after anterior cruciate ligament surgery. Long-term results and outcome predicting factors after primary surgery and late-phase reconstruction. Int J Sports Med. 1996;17(3):223-228.

36. Engelhardt M, Reuter I, Freiwald J. Alterations of the neuromuscular system after knee injury. Eur J Sports Traumatol Rel Res. 2001;23 75-81.

37. Freiwald J, Reuter I, Engelhardt M. Neuromuscular and motor system alterations after knee trauma and knee surgery. A new paradigm. In: Lehmann L, ed. Overload, Performance Incompetence and Regeneration in Sport. New York: Kluwer Academic Press/Plenum Publishers; 1999:81-100.

38. Freiwald J, Engelhardt M. Status of Motor Learning and Coordination in Orthopedic Rehabilitation. Sportorth Sporttraum 2002;18:5-11.

39. Ferber R, Osternig LR, Woollacott MH, Wasielewski NJ, Lee JH. Gait mechanics in chronic ACL deficiency and subsequent repair. Clin Biomech. 2002;17(4):274-285.

Chapter 3Abnormal Landing Strategies after ACL Reconstruction

A. Gokeler, A.L. Hof, M.P. Arnold, P.U. Dijkstra, K.Postema, E. OttenScan J Med Sci Sports 2009; 20: e12–e19

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A B S T R A C T

The objective was to analyze muscle activity and movement patterns during landing of a single leg hop for distance after anterior cruciate ligament (ACL) reconstruction. Nine (six males, three females) patients six months after ACL-reconstruction (ACLR) and 11 (eight males, three females) healthy control (CTRL) subjects performed the hop task. Electromyographic signals from lower limb muscles were analyzed to determine onset time before landing. Biomechanical data were collected using an Optotrak Motion Analysis System and force plate. Matlab was used to calculate kinetics and joint kinematics. Side-to-side differences in ACLR and CTRL subjects as well as differences between the patients and CTRL group were analyzed. In ACLR limbs, significantly earlier onset times were found for all muscles, except vastus medialis, compared with the uninvolved side. The involved limbs had significantly reduced knee flexion during the take-off and increased plantarflexion at initial contact. The knee extension moment was significantly lower in the involved limb. In the CTRL group, significantly earlier onset times were found for the semitendinosus, vastus lateralis and medial gastrocnemius of the non-dominant side compared with the dominant side. Muscle onset times are earlier and movement patterns are altered in the involved limb six months after ACLR.

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I N T R O D U C T I O N

Successful anterior cruciate ligament (ACL) reconstruction in terms of restoring the anterior laxity of the knee joint to near-normal values does not automatically mean restoration of normal knee function.1 For example, only 31% of patients after ACL-reconstruction (ACLR) regain a normal walking pattern one year after surgery.2 Biomechanical analysis of hop tasks revealed persistent altered knee joint moments > one year after ACLR.3 Recent research has shown that the results of hop tests can be used as predictors of short-term dynamic stability in subjects with ACL-deficient (ACLD) knees.4 These tests are appealing as they are easy to perform, simulate in part sport-specific demands and have satisfactory reliability.5

In several papers studying high demand activities of the ACLR knee, substitutions of moments were shown to occur from the knee to the hip or ankle.6,7 The data suggest that the patients used a strategy by transferring the moments from the knee to the hip and/or the ankle in order to reduce the knee moment. The studies cited above, however, lack the incorporation of electromyographic (EMG) data during the hopping tasks.3,6,7 If functional deficits last more than one year after surgery, it is reasonable to assume that deficits are even more pronounced six months after surgery. Thus, if hop tests are used as indicators of the functional performance of patients after ACLR, it is imperative that a comprehensive assessment that includes kinematic, kinetic and EMG-analysis is conducted in order to better understand the biomechanical and neuromuscular profiles.EMG analysis is a method that offers a partial insight into neuromuscular activity. The onset of muscle activity before landing is particularly of interest because it increases the stiffness of the joints.8 This feed-forward mechanism is important as it allows the muscles time to generate force to provide correct lower extremity alignment during landing. Insufficient timing may place the knee in an unfavorable position, increasing the risk of sustaining an ACL (re)injury. So far, research on muscle onset during hop tasks have been performed in ACLD patients or in patients more than one year after reconstructive surgery.9-11 Muscle onset patterns of patients six months after ACLR, at which time return to sports is commonly allowed, are currently unknown.The purpose of this study was, therefore, to assess the bilateral lower limb joint kinematics and kinetics and onset time of EMG activity during the single leg hop test in patients after ACLR during the single leg hop for distance. These data will be compared with a CTRL group.

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M AT E R I A L A N D M E T H O D S

SubjectsNine consecutive patients after ACLR (six males and three females) with a mean age of 28.4 ± 9.7 years were measured 27 ± 1.5 weeks post-operatively. Eleven healthy subjects (eight males and three females) with a mean age of 26.3 ± 5.5 years were used as CTRL. All subjects were level I–II athletes. Level I sports are described as jumping, pivoting and hard cutting sports. Level II sports also involve lateral motion, but with less jumping or hard cutting than level I.12 Inclusion criteria for the patients were: isolated ACL lesion, no major meniscal or cartilage lesion, normal limb alignment as determined on a standardized lower extremity x-ray and defined as an anatomical femoro-tibial axis of between 2° and 7° of valgus and no varus as well as no relevant previous surgery at any other joint of the limbs. Exclusion criteria were joint effusion, varus thrust of the knee, >50% removal of the width of the base of the meniscus, grade 3 rupture of the collateral ligaments, concomitant ligament injuries to the posterolateral or – medial corner, traumatic or degenerative cartilage lesions <2 cm2, surgical procedures or injuries to contralateral limb or any history of neurological, vestibular or visual impairment. An arthroscopically assisted, iso-anatomical two-incision, bone-patellar tendon-bone (BPTB) technique by the same surgeon was performed on all patients.13 All patients followed the same rehabilitation program at the same institution, consisting of immediate weight-bearing, range of motion (ROM) exercises, stationary bicycle training and closed-chain strengthening and coordination exercises. Running was permitted after 12 weeks, progressing to agility and sports-specific drills. Return to unlimited sports was allowed after nine months. The patients completed the IKDC Subjective Knee Evaluation Form and were examined on the test day according to the IKDC Knee Examination Form.14 Laxity testing was performed using the Rolimeter device (AIRCAST Europe, Freiburg, Germany). The medical ethics committee of the University Medical Center Groningen approved the study protocol, and all subjects signed an informed consent before the measurements started.

Single leg hop testAll subjects performed a single leg hop for distance keeping their arms behind the back, and maintained their balance for at least 1s after landing.15 About 5–10 practice trials were performed to familiarize the subjects with the hop task. All subjects subsequently carried out three maximal trials for each limb and they were instructed to jump as far as possible. The subjects were allowed to use their preferred landing technique. The hop was deemed correct by the experimenter if the subject was able to achieve maximal hop distance while maintaining balance for at least 1s after landing. Limb symmetry in

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the ACLR group was calculated by: (maximum hop distance involved limb/maximum hop distance uninvolved limb × 100). The limb symmetry index in the CTRL group was calculated by: (maximum hop distance dominant limb/maximum hop distance non-dominant limb × 100). In the CTRL group, the dominant limb was defined as the one with the furthest hop distance.The maximum hop distance was used to determine the correct take-off position for each limb and was marked with tape on the floor. From this take-off position, the subject was instructed to land onto the centre of the force plate. Maximum distance was used to maximally challenge the dynamic stability of the knee for this task.16 It was demonstrated in recent research that using the maximal hop test results in a high ability to discriminate between the hop performance of the involved and the uninvolved side both in patients with an ACL injury and in patients who have undergone ACLR.15 All subjects jumped wearing their own sport shoes. Ten correct recordings were obtained for each limb. All subjects took a standardized rest period of 1 min after the third and sixth jump.

BiomechanicsThe set-up for collection of biomechanical data has been described previously and will be summarized here briefly.17 A 3D motion analysis system (OPTOTRAK® Northern Digital Inc., Waterloo, California, USA) with two cameras was used for the acquisition of kinematic data by detecting reflective markers placed on the pelvis and limbs. Sample frequency was 150 Hz. During six phases of the hop, the joint angles for the hip, knee and ankle joints were recorded; phase 1): initiation of take-off, phase 2): moment of toe off, phase 3): flight phase, phase 4): is where initial contact was made on the force plate, phase 5): landing with full body weight; and phase 6): 1s period after initial contact. ROM was operationalized as the difference between the minimum and maximum joint angles and was calculated for the take-off phase and the landing phase.The kinetic variables that were evaluated included vertical end horizontal ground reaction force (GRF) and joint moments. The GRF was normalized to body weight and moments were normalized for body weight × limb length to make comparison between subjects possible. All analyses for moments and angles were performed in the anatomical sagittal (xy) plane and are counted as positive for flexion angles and extension moments. All positive ankle angles are plantar flexion angles. The start of rise in the vertical GRF was used to determine the first instant of the landing. The support moment (Ms) was calculated according to Hof:18

MS = ½ Mhip + Mknee + ½ Mankle = qFp

The kinematic and kinetic variables were imported and calculated in the Matlab (The Mathworks Inc., Natick, Massachusetts, USA) toolbox in BodyMech (BodyMechGuide

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3.06.01, Version 2006, http://www.bodymech.nl). A biomechanical analysis was performed on all patients. Unfortunately, we lost part of the biomechanical data in the first four patients as marker recognition was erroneous due to daylight in the lab. Hence, due to an incomplete set of data and insufficient number files, a statistical analysis could not be performed. Owing to time restrictions of the principal investigator, more patients could not be included for the current paper.

EMGEMG data of the following limb muscles were recorded: gluteus maximus (GM), biceps femoris (BF), semitendinosus (ST), semimembranosus (SM), vastus medialis (VM), vastus lateralis (VL), rectus femoris (RF), gastrocnemius medial and lateral head (MG and LG) and soleus (SO). After skin preparation, disposable surface electrodes (Neotrode®, Conmed Corporation, Utica, New York, USA) with a 10 × 10 mm electrode area were placed with an interelectrode distance of 20 mm. The electrode pair was positioned in the longitudinal direction of the muscle fibers in accordance with SENIAM guidelines.19 EMGs were recorded with a PORTI (Twente Medical Instruments, Enschede, the Netherlands) physiologic data logger, which was connected by a fiber-optic cable to the computer. Pre-amplifier specifications were >110 dB common mode rejection, <2 μV RMS noise level and >500 MΩ input impedance. The pre-amplified EMGs were sampled at 800 Hz and high-pass filtered at 20 Hz with a third-order digital Butterworth filter.The force plate signal was sampled at 750 Hz and used for the kinematic and kinetic analysis. An analogue trigger circuit was connected to the vertical GRF output, using a trigger level of approximately 100 N. This trigger signal was recorded, together with the EMGs, on the EMG recording device. The latter had a sampling frequency of 800 Hz, but was asynchronous with the kinematic data acquisition. For the detection of the onset times τ, the “approximated generalized likelihood ratio” (AGLR) was used.20 In this test, the ratio (variance after t=τ)/(variance before t=τ) is determined for all possible values of τ over a sensible interval. The value of τ at which the logarithm of this ratio is maximal is selected as the most probable onset time. Identification of this point allowed to differentiate between activity shortly after take-off and the preparatory activity before landing. The latter was of interest in this study and was defined as onset time.In our experiments, we first calculated the smoothed (10 Hz zero-lag Butterworth filter) rectified EMG. The square of two × its minimum value over the interval (0.5–0 s) before landing was taken as the “variance before.” The start of the “sensible interval” was the interval before landing over which the smoothed rectified EMG remained below three × the minimum value. The duration of this interval was 1 s. The onset time is the continuous rise in EMG activity as defined by the algorithm, indicating the build-up of muscle activity preparing for landing.

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Statistical analysisThe mean onset times of the EMG signals for each muscle were calculated. Differences between uninvolved and involved limbs in the ACLR and differences between dominant and non-dominant limbs in the CTRL group were analyzed using the Wilcoxon signed ranks test. The Mann–Whitney test for independent samples was used to analyze leg differences in onset times between ACLR and CTRL groups, α-levels were set at < 0.05 for statistical significance. For each kinematic and kinetic variable, mean values from five jumps were compared between the involved and the uninvolved limbs of all patients. The mean difference was used for statistical analysis with a non-parametric Wilcoxon signed ranks test.

R E S U LT S

IKDCThe mean subjective IKDC score for the ACLR was 81 ± 7.1. The objective IKDC score revealed that one patient had an A, seven had a B and one patient scored a C (donor site pain on palpation). Mean laxity showed <2 mm side-to-side difference. All patients had negative Lachman and pivot shift test results. Meniscus lesions were found in all patients, equally divided in four medial and four lateral meniscus lesions, all requiring partial meniscectomy. In one patient there was a combined lesion of the medial meniscus + grade II chondral lesion of the medial femoral condyle.

Hop indexThe mean limb symmetry index for the CTRL was 95.5. The mean distance of the dominant limb was 143.0 ± 6.8 cm vs 136.8 ± 5.7 cm of the non-dominant limb. The limb symmetry index for the patients was 83.8, with a mean distance for the involved of 93.7 ± 19.2 cm and 111.7 ± 8.2 cm for the uninvolved limbs, respectively.

BiomechanicsKinematicsThe involved limbs had significantly reduced knee flexion during the take-off phase and more plantar flexion in the ankle at initial contact when compared with the uninvolved side. Knee ROM of the involved limb was significantly decreased during take-off in comparison with the uninvolved side. There was a trend that ROM was decreased for the hip and ankle joint in the involved limb during take-off. During the landing phase, there was a trend that ROM was decreased for the hip and knee joint and increased in the ankle joint of the involved limb compared with the uninvolved side (Table 1).

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Table 1. Mean hip, knee and ankle angles (SD) of the involved and uninvolved limb for each hop phase of all subjects. These phases are: 1 = before take-off, 2 = take-off, 3 = flight, 4 = initial contact, 5 = landing, 6 = 1 sec after initial contact. Range of motion (SD) of the involved and uninvolved limb during take-off (ROM1) and landing (ROM2). ROM angles for take-off are the differences between joint angles of phase 1 and phase 2. ROM angles for landing are the differences between joint angles of phase 4 and phase 5.

Hop phases

Hip Knee Ankle

Uninvolved (SD)

Involved (SD) p Uninvolved

(SD)Involved (SD) p Uninvolved

(SD)Involved (SD) p

1 65.7 (16.9) 75.7 (41.4) 0.90 61.9 (6.6) 50.6 (5.7) 0.04 -23.3 (5.0) -15.9 (10.2) 0.08

2 8.3 (4.45) 13.5 (5.2) 0.08 24.9 (5.3) 26.5 (6.4) 0.50 16.0 (4.6) 12.7 (12.6) 0.80

3 32.6 (7.6) 31.5 (3.9) 0.90 54.2 (4.2) 49.9 (7.0) 0.08 15.6 (6.7) 23.1 (12.0) 0.30

4 51.7 (10.4) 46.6 (6.9) 0.50 16.1 (3.8) 14.8 (4.7) 0.70 0.4 (2.7) 15.9 (13.4) 0.04

5 71.1 (9.4) 59.5 (11.4) 0.08 58.4 (7.5) 46.6 (6.4) 0.08 -3.4 (3.9) 3.6 (13.2) 0.70

6 52.3 (13.5) 42.6 (18.4) 0.10 32.9 (11.5) 31.2 (12.1) 0.70 -2.7 (3.1) 2.3 (17.1) 0.90

ROM take-off

57.6 (20.0) 62.2 (11.4) 0.08 37.0 (8.8) 25.3 (4.9) 0.04 39.3 (7.9) 28.4 (5.6) 0.08

ROM landing

18.8 (6.2) 13.7 (7.0) 0.20 42.3 (5.1) 31.3 (7.3) 0.08 5.7 (2.1) 13.3 (11.0) 0.30

KineticsThe horizontal GRF was significantly lower in the involved limbs compared with uninvolved limbs (Table 2). There was no significant difference between limbs for vertical GRF. The mean knee extension moment was significantly lower in the involved limb. Hip extension and ankle plantarflexion moments were increased on the involved side, but not statistical significant. The support moment was significantly lower for the involved limbs. Compensation for the reduced knee extension moment was primarily made at the ankle joint.

Table 2. Mean normalized peak ground reaction force (GRF), peak internal hip, knee, ankle and support extensor moments in landing, standard deviation (SD) and significance level.

Mean uninvolved (SD) Mean involved (SD) p

Horizontal GRF (N/BW) 0.89 (0.23) 0.74 (0.26) 0.01

Vertical GRF (N/BW) 2.17 (0.23) 2.24 (0.36) 0.80

Hip (Nm/BW/limb length) 0.25 (0.07) 0.29 (0.08) 0.90

Knee (Nm/BW/limb length) 0.30 (0.03) 0.17 (0.05) 0.04

Ankle (Nm/BW/limb length) 0.12 (0.03) 0.14 (0.03) 0.10

Support moment (Nm) 0.37 (0.03) 0.30 (0.01) 0.04

The observation that the horizontal GRF is lower in the involved limb can partly be clarified by a biomechanical analysis of the movement, using a 2D 8-segment model with turning joints.21 The inverse dynamics simulation was performed on a particular jump on an involved limb, that is: the joint angles, velocities and accelerations were derived

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from the recordings. The ground contacts and the GRF were calculated from forward dynamics simulation (Figure 1(a)).21 In a second simulation, the movement of the swing of the lower limb was reduced during landing, so that its foot would not pass the stance foot (Figure 1(b)). From this simulation, it appeared that the horizontal component of the GRF was reduced in the first simulation by the ongoing swing of the lower limb compared with the second simulation. As can be seen from Figure 1(a), the distance between the GRF and the knee joint is kept very small, indicating a low knee extensor moment. This indicates that the landing strategy incorporates the swing limb in keeping knee extensor torques limited. It also suggests that the adapted movement control pattern covers at least both limbs.

Figure 1. Landing phase of the involved limb derived from a 2D simulation. The effect of the contralateral swing limb is shown. The line shows the attachment point and direction of the ground reaction force (GRF). (a) The swing limb passes the stance limb resulting in distance of the GRF close to the knee joint. This results in a lower knee extension moment. (b) The swing limb remains behind the stance limb resulting in a distance of the GRF further away from the knee joint. The knee extension moment is increased.

EMGOnset timesEMG onset times in patients of the GM, BF, ST, SM, VL, RF, MG, LG and SO muscles were significantly earlier in the involved limb (Table 3). The earlier onset time for the VM was, however, not significantly different in the involved limb. EMG onset times in healthy subjects of the different muscles did differ significantly between dominant and non-dominant sides, except for the ST, VL and MG, which were significantly earlier in the non-dominant limbs. Differences in EMG onset times between the involved and the uninvolved side in the ACLR group were significantly larger than differences between the dominant and the non-dominant side in CTRL group, except for the ST, VL and VM (Table 3). Most muscles in the uninvolved side had later onset times when compared with the involved side in patients after ACLR.

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Tabl

e 3.

Mea

ns a

nd d

iffer

ence

s in

mea

ns in

EM

G on

set ti

mes

(ms)

of h

ealth

y su

bjec

ts (d

omin

ant a

nd n

on d

omin

ant l

imbs

) and

of p

atien

ts (u

ninv

olve

d lim

bs a

nd

invo

lved

). Di

ffere

nces

bet

wee

n lim

bs w

ere

com

pare

d be

twee

n he

alth

y su

bjec

ts a

nd p

atien

ts. A

bbre

viati

ons:

(GM

) glu

teus

max

imus

, (BF

) bic

eps f

emor

is, (S

T)

sem

itend

inos

us, (

SM) s

emim

embr

anos

us, (

VM) v

astu

s med

ialis

, (VL

) vas

tus l

ater

alis,

(RF)

rect

us fe

mor

is, (M

G an

d LG

) gas

troc

nem

ius m

edia

l and

late

ral h

ead

and

(SO

) sol

eus.

Mus

cles

U

ninv

olve

d le

g pa

tient

s (SD

)In

volv

ed le

g pa

tient

s (SD

)

Mea

n di

ffere

nce

un

invo

lved

-in

volv

ed li

mb

patie

nts (

SD)

pDo

min

ant l

eg

cont

rols

(SD)

Non

dom

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t le

g co

ntro

ls

(SD)

Mea

n di

ffere

nce

dom

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t - n

on-

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ls (S

D)

pM

ean

diffe

renc

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ls –

pati

ents

P

GM76

.4 (3

4.4)

124.

6 (2

0.7)

-48.

2 (3

7.5)

0.02

106.

3 (2

3.6)

103.

0 (2

5.4)

-3.3

(9.4

)0.

10-5

1.5

0.00

1

BF90

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0.2)

119.

7 (2

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-28.

9 (3

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0.02

91.4

(20.

6)95

.6 (1

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4.2

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30-2

4.7

0.01

ST95

.0 (4

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120.

8 (1

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-25.

8 (3

3.1)

0.04

105.

8 (1

4.6)

110.

7 (1

4.5)

4.8

(8.8

)0.

03-2

1.0

0.80

SM90

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124.

4 (1

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-33.

6 (3

3.0)

0.01

101.

4 (1

9.6)

107.

2 (1

5.5)

5.8

(15.

5)0.

30-2

7.8

0.01

VL70

.9 (3

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90.6

(18.

4)-1

9.7

(65.

5)0.

0291

.6 (2

9.5)

100.

7 (3

2.4)

-9.1

(19.

5)0.

04-1

0.5

0.30

VM73

.1 (3

9.4)

110.

8 (1

6.3)

-37.

7(39

.8)

0.10

95.1

(28.

6)11

2.8

(27.

7)-1

7.7

(19.

6)0.

30-2

0.1

0.50

RF58

.1 (2

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83.5

(12.

3)-2

5.4

(31.

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.7 (1

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66.5

(10.

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.2 (1

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0.40

-29.

60.

01

MG

46.7

(27.

8)86

.7 (4

2.0)

-40.

0 (3

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0.03

62.2

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3)64

.4 (1

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2.2

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04-3

7.8

0.00

6

LG55

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4.3)

103.

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0.9)

-48.

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0.01

61.9

(15.

7)65

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3.8)

3.8

(11.

1)0.

10-4

4.6

0.05

SO50

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1.2)

101.

0 (1

7.0)

-51.

0 (2

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59.9

(13.

7)61

.2 (1

1.5)

1.3

(7.1

)0.

10-4

9.7

0.00

2

Abnormal Landing Strategies after ACL Reconstruction

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3

37

D I S C U S S I O N

Six months after ACLR, muscle onset times of the GM, VL, RF, BF, SM, MG, LG and SO of the involved limb were significantly earlier before landing. This indicates that patients, unconsciously or consciously, increase the pre-tension of the limb muscles before the landing of a single leg hop test. These findings are in agreement with a study showing that muscle pre-activity increases the sensitivity of the muscle spindles, allowing joint perturbation to be detected more quickly.22 Patients in the current study appear to utilize a distinctive feedforward control strategy that enhances joint stability. In fact, this was found in the biomechanical part of this study that was conducted on five of the nine patients reported. The patients had decreased knee flexion angles and moments at landing in the involved limb. Hence, the patients stiffened the involved limb before and during landing. These findings reinforce the fact that preparatory muscle activity results in increased joint stability.23 Stability in this respect is the state of a joint remaining or promptly returning to proper alignment through an equalization of forces. Earlier onset times of the hamstrings were noted in the current experiment. Earlier activity of the BF has also been reported during a drop jump.10 Unfortunately, these authors reported only the total mean time of both limbs; hence, the contribution of the involved limb could not therefore be discerned from their results. Others have not found differences in the EMG activity of the hamstrings when comparing patients after ACLR with uninjured subjects during a single leg hop.24 The explanations for the differences could be the time between surgery and the jump task, EMG analysis technique and gender of subjects.The VL and RF had earlier onset times in the involved limb, which is in agreement with others, but again only the total means of both limbs in patients after ACLR were reported in that study.10 Earlier EMG onset time of the LG of the involved limb found in this study has been reported in female ACLR and in patients with ACLD9,25 In general, it is remarkable that patients after ACLR had earlier EMG onset times. The patients after ACLR in this paper had shorter jump distances, and yet had earlier EMG onset times outside the normal values as demonstrated in CTRL. They fired the muscles sooner relative to the time of landing. We want to reiterate how we defined muscle onset time: the first burst in EMG as detected by Staude and Wolf algorithm before landing. This definition is in agreement with others.26 The rise in muscle activity has been shown to be timed relative to the expected time of landing and not the point of take-off.26 Visual estimation of the jump distance might provide the necessary input to predict jump and scaling of the muscle activity. In case the jump distance was increased, the onset of EMG remained practically the same relative before landing. Sensorimotor memories of the dynamic interactions between the body and the environment have been shown to provide a robust mode of motor control. It may be that patients have adapted, based on

Chapter 3

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the negative experiences such as giving way of the knee before surgery, or modified their motor programming, e.g., by limiting the amount of flexion in the knee upon landing. Before landing, they demonstrated a general co-contraction of the muscles to “tense up” before foot contact occurred in an attempt to increase the stability of the knee.27

Interestingly, muscle onset in most muscles of the uninvolved limb of the patients after ACLR was in fact later when compared with the CTRL group. We can only speculate on this finding. Perhaps, the patients after ACLR had ineffectively timed neuromuscular firing before sustaining the ACL injury. Although speculative, this is an issue of concern, as late muscle onset might increase the risk of ACL injury.28 Recently, subjects with an ACLD knee who experience instability of the knee during daily activities or sports have been classified as non-copers.29 These non-copers have abnormal movement patterns of the knee as well as altered neuromuscular control.30 Presumably, although the patients had surgical reconstruction of the ACL, they still show some typical muscle activity patterns that have been reported in non-copers.31,32 The patients after ACLR as well as non-copers utilize a stabilization strategy, that stiffens the knee joint. Another possibility is that the adaptations in fact were learned early in the rehabilitation to protect the donor site. It may require more time than the six months after the reconstruction to “reprogram” the neuromuscular system. The present results are in agreement with other reports following ACLR, indicating that the movement patterns are altered during functional tasks and these last beyond the time frame when return to sports is allowed.3,6,7,33-35 Paterno and co-workers showed that female patients after ACLR had higher vertical GRF on the uninvolved side during a drop vertical jump.35 In other words, patients loaded their uninvolved side more than the involved side until a mean of 27 months after surgery. Residual asymmetries at a mean time of 7.2 years after ACLR were also found in another cohort of female ACLR.34 They reported greater co-contraction ratios of the hamstrings–rectus femoris and decreased peak anterior–posterior shear force during a drop jump in comparison with healthy subjects. Considering that injury risk is increased five-fold soccer players after ACLR in comparison with uninjured players,36 rehabilitation programs may need to be extended or revised to prevent recurrent injury.The number of patients available for this study was limited to nine. Before this study, a power analysis could not be conducted based on the literature due to absence of numerical data,9 data for both involved and uninvolved limbs were grouped into one figure,10 or data from the involved limb of patients with ACLD11 were reported. The strength of the limb muscles had not been tested in this study. This limitation is of minor influence, because quadriceps strength has only a low correlation to hopping performance after ACLR.37

Abnormal Landing Strategies after ACL Reconstruction

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The sole use of the single limb hop test for distance to decide whether return to high demand sports is safe for patients after ACLR may be questioned. The patients did not fulfill the demanded limb symmetry of >85% as one of the criteria to return to sports as proposed in the literature.38 The mean maximum hop limb symmetry was 83.8 and was based on maximum distance achieved and not on the average of three hops. It has been shown from the literature that average results from the hop test underestimate the potential in patients.5,39 Patients show an increase in jump distance as trials progresses. They even improve jump distance from trial to trial, which is not seen in healthy controls.39 Secondly, it was demonstrated in a recent research that using the maximal hop test results in a high ability to discriminate between the hop performance of the involved and the uninvolved side both in patients with an ACL injury and in patients who have undergone ACLR.15 One should keep in mind that our patients had been treated with a BPTB technique; it is possible that the results might differ had a different ACL graft been used. It is recognized that the hop task as used in this study is a pre-planned activity, but was chosen for its high reliability.5 On the other hand, it would be interesting to repeat a jump task experiment with patients after ACLR under unanticipated or fatigued conditions to simulate normal athletic activity. It has been shown that unanticipated cutting tasks lead to a non-specific co-contraction of the muscles to increase joint stiffness.40 This phenomenon is basically what patients in the current study demonstrated. Recently, Wilkstrom et al. demonstrated altered muscle onset times in jump trials in which subjects were not able to maintain balance upon landing.41 Their paper indicated that successful jump landing required an earlier muscle activity in order to land safely.

PerspectivesIt is remarkable that, although anterior laxity has been (nearly) restored, patients after ACLR still utilize muscle recruitment patterns to increase the stiffness of the knee similar to patients with ACLD knees.42 Movement patterns in the involved limbs were also significantly different from uninvolved limbs. Moreover, they do this by including the control of the swing leg during landing, according to our biomechanical simulations. The asymmetries in muscle onset and movement patterns may predispose to re-injury of the ACL. Future studies with a prospective and longitudinal design should focus on whether and how these asymmetries may change over time and whether they can be improved by rehabilitation. Furthermore, sensitive tests should be developed to determine a safe return to sports.

Chapter 3

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AcknowledgementsThe authors thank Anne Benjaminse P.T. of the Neuromuscular Research Laboratory of the University of Pittsburgh for her assistance with the preparation of the manuscript. In addition, we thank Alieke Drok M.A., who assisted with the measurements as part of fulfillment of her research thesis at the Center for Human Movement Science at the University of Groningen in the Netherlands.

Abnormal Landing Strategies after ACL Reconstruction

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R E F E R E N C E S1. Dye SF. The knee as a biologic transmission with an envelope of function: a theory. Clin Orthop Relat Res.

1996(325):10-18.

2. Schmalz T, Blumentritt S, Wagner R, Junge R. [Evaluation with biomechanical gait analysis of various treatment methods after rupture of the anterior cruciate ligament]. Sportverletz Sportschaden. 1998;12(4):131-137.

3. Decker MJ, Torry MR, Noonan TJ, Riviere A, Sterett WI. Landing adaptations after ACL reconstruction. Med.Sci.Sports Exerc. 2002;34(9):1408-1413.

4. Fitzgerald GK, Lephart SM, Hwang JH, Wainner RS. Hop tests as predictors of dynamic knee stability. J Orthop Sports Phys Ther. 2001;31(10):588-597.

5. Clark NC. Functional performance testing following knee ligament injury. Phys Ther Sport. 2001;2 (2):91-105.

6. Ernst GP, Saliba E, Diduch DR, Hurwitz SR, Ball DW. Lower extremity compensations following anterior cruciate ligament reconstruction. Phys Ther. 2000;80(3):251-260.

7. Webster KE, Gonzalez-Adrio R, Feller JA. Dynamic joint loading following hamstring and patellar tendon anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2004;12(1):15-21.

8. Solomonow M, Krogsgaard M. Sensorimotor control of knee stability. A review. Scand J Med Sci Sports. 2001;11(2):64-80.

9. DeMont RG, Lephart SM, Giraldo JL, Swanik CB, Fu FH. Muscle Preactivity of Anterior Cruciate Ligament-Deficient and -Reconstructed Females During Functional Activities. J Athl Train. 1999;34(2):115-120.

10. Pfeifer K, Banzer W. Motor performance in different dynamic tests in knee rehabilitation. Scand J Med Sci Sports. 1999;9(1):19-27.

11. Smith J, Malanga GA, Yu B, An KN. Effects of functional knee bracing on muscle-firing patterns about the chronic anterior cruciate ligament-deficient knee. Arch Phys Med Rehabil. 2003;84(11):1680-1686.

12. Daniel DM, Stone ML, Dobson BE, Fithian DC, Rossman DJ, Kaufman KR. Fate of the ACL-injured patient. A prospective outcome study. Am J Sports Med. 1994;22(5):632-644.

13. Arnold MP, Verdonschot N, van Kampen A. ACL graft can replicate the normal ligament’s tension curve. Knee Surg Sports Traumatol Arthrosc. 2005;13(8):625-631.

14. Irrgang JJ, Anderson AF, Boland AL, et al. Responsiveness of the International Knee Documentation Committee Subjective Knee Form. Am J Sports Med. 2006;34(10):1567-1573.

15. Gustavsson A, Neeter C, Thomee P, et al. A test battery for evaluating hop performance in patients with an ACL injury and patients who have undergone ACL reconstruction. Knee Surg Sports Traumatol Arthrosc. 2006;14(8):778-788.

16. Clark NC, Gumbrell CJ, Rana S, Traole CM, Morrissey C. Intratester reliability and measurement error of the adapted crossover hop for distance. Phys Ther Sport. 2002;3(3):143-151.

17. van der Harst JJ, Gokeler A, Hof AL. Leg kinematics and kinetics in landing from a single-leg hop for distance. A comparison between dominant and non-dominant leg. Clin Biomech. 2007;22(6):674-680.

18. Hof AL. On the interpretation of the support moment. Gait.Posture. 2000;12(3):196-199.

19. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J.Electromyogr.Kinesiol. 2000;10(5):361-374.

20. Staude G, Wolf W. Objective motor response onset detection in surface myoelectric signals. Med.Eng Phys. 1999;21(6-7):449-467.

21. Otten E. Inverse and forward dynamics: models of multi-body systems. Philos Trans R Soc Lond B Biol Sci. 2003;358(1437):1493-1500.

22. Dyhre-Poulsen P, Simonsen EB, Voigt M. Dynamic control of muscle stiffness and H reflex modulation during hopping and jumping in man. J.Physiol. 1991;437:287-304.

23. Riemann BL, Lephart SM. The Sensorimotor System, Part I: The Physiologic Basis of Functional Joint Stability. J Athl Train. 2002;37(1):71-79.

Chapter 4Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant? A Systematic Review

A. Gokeler, A. Benjaminse, T.E. Hewett, S.M. Lephart, L. Engebretsen, E. Ageberg, M. Engelhardt, M.P. Arnold, K. Postema, E. Otten, P.U. Dijkstra

Br J Sports Med 2012; 46(3):180-192

Chapter 4

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A B S T R A C T

Objective: To establish the clinical relevance of proprioceptive deficits reported after anterior cruciate ligament injury (ACL).Material and Methods: A literature search was done in electronic databases from January 1990 to June 2009. Inclusion criteria for studies were ACL-deficient (ACLD) and ACL-reconstructed (ACLR), articles written in English, Dutch or German and calculation of correlation(s) between proprioception tests and clinical outcome measures. Clinical outcome measures were muscle strength, laxity, hop test, balance, patient reported outcome, objective knee score rating, patient satisfaction or return to sports. Studies included in the review were assessed on their methodological quality. Results: In total 1161 studies were identified of which 24 met the inclusion criteria. Pooling of all data was not possible due to substantial differences in measurement techniques and data analysis. Most studies failed to perform reliability measurements of the test device used. In general the correlation between proprioception and laxity, balance, hop tests and patient outcome was low. Four studies reported a moderate correlation between proprioception, strength, balance or hop test. Conclusion: There is limited evidence that proprioceptive deficits as detected by commonly used tests adversely affect function in patients after ACLD and ACLR. Development of new tests to determine the relevant role of the sensorimotor system are needed. These tests should ideally be used as screening test for primary and secondary prevention of ACL injury.

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

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45

I N T R O D U C T I O N

The anterior cruciate ligament (ACL) is the most commonly injured ligament in the body.1 Instability of the knee often occurs after ACL injury in pivoting type sports and ACL-reconstruction (ACLR) often is recommended.2 Nonetheless, despite ACLR, up to a third of patients will not reach their pre-injury activity level,3 which may be attributed to fear of re-injury.4 Of concern is the incidence of recurrent injury to the operated knee ranging from 3,6% 5 in adults to 17% in patients under 18 years of age.6 An ACL injury increases the risk of osteoarthritis with a prevalence ranging from 0% to 13% for patients with isolated ACL-deficient (ACLD) knees and 21% to 48% for patients with combined injuries.7 Proprioceptive deficits after ACL injury may be a factor related to both giving way and higher incidence of subsequent injuries, which in turn may contribute to the development of osteoarthritis.8 Proprioceptive deficits are claimed to adversely affect activity level,9-11 balance,12,13 re-establishment of quadriceps strength14 and increase the risk of further injury.15 Evidence supporting such claims is not readily available as was revealed by an earlier critical review on this topic.16 The objective of this review is to analyze the correlations between proprioception in patients after ACLD and ACLR and common clinical outcome measurements such as objective scores, strength, laxity, balance, hop tests and patient reported outcomes.

M AT E R I A L S A N D M E T H O D S

An electronic search was performed in Medline, Cinahl and Embase on studies published between January 1990 and June 2009. In addition, a manual search was conducted by tracking the reference lists of the included studies. The inclusion criteria in this review were: 1) studies reporting on patients with a rupture of the ACL diagnosed by positive Lachman, pivot shift, KT-1000, MRI or arthroscopy; 2) studies reporting on ACLR using an autograft or allograft; 3) proprioception measures; 4) full text published in English, Dutch or German; 5) outcome measures classified to the World Health Organization (WHO) including a) impairment of body functions: strength, laxity; b) activity limitation: hop test, balance; c) participation restriction: objective or patient reported outcome and 6) correlation reported between proprioceptive tests and outcome measurements as listed above. For this review, the two most commonly methods to quantify proprioception were included. These were defined at the Foundation of Sports Medicine Education and Research Workshop in 1997 as: joint position sense (JPS) and threshold to detection of passive motion (TTDPM).17 JPS is assessed by measuring reproduction of passive

Chapter 4

46

positioning (RPP) or active repositioning of the knee (RAP). Studies that analyzed other forms of proprioception were excluded in this review due to reported decreased accuracy.18 The search terms are presented in Table 1.

Table 1. Search terms used in the databases of Medline, Embase and Cinahl from January 1990-June 2009. (MeSH, medical subject heading; TI, title; ti,ab, title abstract, MH, medical heading; TX, text)

Medline Embase Cinahl

1 “proprioception” [MeSH] ‘proprioception’ exploded proprioception MH

2 “mechanoreceptors” [MeSH] ‘kinesthesis’ exploded somatosensory disorders MH

3 “sensory thresholds” [MeSH] ‘somatosensory’ exploded kinesthesis MH

4 “kinesthesis” [MeSH] ‘mechanoreceptors’ exploded receptors, sensory MH

5 proprioception [TI] ‘proprioception’ in ti,ab mechanoreceptors MH

6 mechanoreceptors [TI] ‘proprioceptive’ in ti,ab proprioception TX

7 kinesthesis [TI] ‘kinesthesis’ in ti,ab proprioceptive TX

8 kinesthesia [TI] ‘kinesthesia’ in ti,ab kinesthesis TX

9 joint position sense [TI] kinesthetic’ in ti,ab kinesthesia TX

10 “anterior cruciate ligament” [MeSH]

‘somatosensory’ in ti,ab kinesthetic TX

11 “knee joint” [MeSH] ‘mechanoreptors’ in ti,ab somatosensory disorders TX

12 ACL injury [TI] ‘sensory receptors’ in ti,ab mechanoreceptors TX

13 ACL deficient [TI] ‘ligament’ exploded sensory receptors TX

14 ACL reconstruction [TI] ‘knee’ exploded joint position sense TX

15 ‘joint’ exploded motion perception TX

16 anterior cruciate ligament MH

17 knee joint MH

18 anterior cruciate ligament TX

19 ACL TX

20 ACL deficient TX

21 ACL injury TX

22 ACL reconstruction TX

23 (#1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7 OR #8 OR #9) AND (#10 OR #11 OR #12 OR #13 OR #14)

(#1 OR #2 OR #3 OR #4 OR #5 OR #6 OR #7 OR #8 OR #9 OR #10 OR #11) AND (#12 OR #13 OR #14 OR #15)

(#1 or #2 or #3 or #4 or #5 or #6 or #7 or #8 or #9 or #10 or #11 or #12 or #13 or #14 or #15) AND (#16 or #17 or #18 or #19 or #20 or #21 or #22)

A modified version of the Cochrane Methods Group on Screening and Diagnostic Tests Methodology (CM) was used to assess the methodological quality.19 The following criteria were modified: questions 1-4 were replaced by Oxford Center For Evidence-based Medicine (http:www.cebm.net.index.aspx?0=1025) to score the level of evidence from 1 to 5. Level 1 is the highest score and level 5 the lowest score possible. Questions pertaining to inclusion criteria, study design, setting, previous tests/referral time since

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

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47

injury or surgery, co-morbid conditions, description of index test (JPS and TTDPM) and its reproducibility, demographic information, percentage missing were used and a question was added regarding statistical analysis. The maximum score of the modified CM was 16 points.

In addition, effect sizes (ES), were calculated where d=0.2-0.5, d=0.5-0.8 and d≥0.8 representing a small, moderate and large effect respectively.20 Correlation coefficients were interpreted as r = 0-0.25 as ‘no correlation’, r = 0.26-0.49 as ‘low’, r = 0.50-0.69 as ‘moderate’, r = 0.70-0.89 as ‘good’ and r = 0.90-1.0 as ‘excellent’. A total of 1161 studies were identified in the databases and 48 duplicates were discarded leaving 1113 studies. Seven studies were retrieved by manual search. Of the total of 1120 studies, four were excluded because of language restrictions.21-24 From the 1116 studies, 83 which were identified as potentially relevant after reading the abstract. The full text of these 83 studies were independently assessed by two observers (AG and AB) after which 59 studies were excluded as they did not meet the inclusion criteria. A consensus meeting was needed on four studies.25-28 Hence, in total 24 studies were included; 20 of which were cross-sectional 25,26,28-44 and four had a prospective design.8,45-47 Reliability was reported in 12 studies,8,26,29,31,34,39-42,44,47,48 of which six were conducted at the same center.8,29,34,41,42,45 In seven studies the same, or part of the patient population was measured but different outcome measures were presented.8,26,29,31,41,42,45 In six studies data on correlation was not provided and the principal author from each study was contacted with a request to provide data , one replied but was not able to provide data,9

four provided data,29,30,39,41 and one author did not reply despite two contact attempts.47

R E S U LT S

The methodological quality is presented in Table 2. The mean score on the CM was 8 ± 2 and none of the reviewed studies scored higher than level 5 evidence. Table 3 summarizes the characteristics of included patients.

Chapter 4

48

Tabl

e 2.

Met

hodo

logi

cal a

sses

smen

t.

Auth

ors

1.

Desig

n2.

Le

vel o

f ev

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3. Sel

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n cr

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cle

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9.

Desc

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n of

inde

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st

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the

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Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

49

Tabl

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Met

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t (Co

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th

e in

dex

test

is b

eing

ev

alua

ted

(sym

ptom

atic

or

asym

ptom

atic

patie

nts)

(1

poi

nt)

mea

n or

m

edia

n an

d SD

re

port

ed

(1 p

oint

)

deta

ils

give

n (1

poi

nt)

age

(mea

n or

m

edia

n an

d SD

or r

ange

) an

d ge

nder

re

port

ed

(1 p

oint

)

test

dev

ice,

patie

nt

positi

onin

g,

spee

d te

sted

, nu

mbe

r of

tria

ls(tw

o or

mor

e ite

ms

1 po

int )

deta

ils g

iven

on

mea

n or

m

edia

n, S

D or

CI

and

p-v

alue

pr

oprio

cepti

ve

test

s and

p-

valu

e co

rrel

ation

(1

poi

nt)

relia

bilit

y re

port

ed

(1 p

oint

)

all i

nclu

ded

subj

ects

m

easu

red

and

if ap

prop

riate

: m

issin

g da

ta o

r w

ithdr

awal

s fro

m st

udy

repo

rted

or

expl

aine

d(1

poi

nt)

Frem

ery

et a

l. (2

000)

11

01

11

11

10

01

9

Birm

ingh

am e

t al

. (2

001)

0

10

11

10

11

10

18

Adac

hi e

t al.

(200

2)0

10

11

00

01

00

15

Reid

er e

t al.

(200

3)

11

11

10

10

10

11

9

Kata

yam

a et

al.

(200

4)0

10

11

01

01

10

17

Robe

rts e

t al.

(2

004)

0

10

11

11

01

11

19

Ageb

erg

et a

l. (2

005)

0

11

11

10

11

11

110

Robe

rts e

t al.

(2

007)

0

10

11

01

11

11

19

Ageb

erg

and

Frid

en (2

008)

1

11

11

11

11

11

112

Zhou

et a

l. (2

008)

0

11

11

11

11

11

111

Lee

et a

l. (2

009)

01

01

11

11

11

01

9M

uaid

i et a

l. (2

009)

01

01

11

01

11

11

9

Mea

n (S

D)8

(2)

Chapter 4

50

Table 3. Demographics of subjects.

Author n ACL Age (SD) n C Age

(SD) Design Time from injury (SD) Additional injury

ACL-D

Corrigan et al. (1992)

20 (11 analyzed)

30 (N.R.) 17 28 (N.R.) c 5.3 (N.R) years N.R.

Wright et al. (1995)

9 18-40 (N.R.) 15 18-40 (N.R.)

c 8,7 (N.R.) months 1 meniscus lesion

Borsa et al. (1997)

29 28.7 (1.7) c 41.7 (11.7) months

5 meniscus and 2 MCL grade III lesions

Borsa et al. (1998)

29 28.7 (N.R) c 41.7 (11.7) months

5 meniscus and 2 MCL grade III lesions

Friden et al. (1998)

17 28 (N.R.) 40 25 (N.R.) c N.R N.R.

Beynnon et al. (1999)

20 40 (7.4) c 5.5 (6.5) years 6 meniscus lesions

Friden et al. (1999)

16 26 (N.R) l 1,2 and 8 (N.R.) months

15 meniscus, 8 MCL and 4 chondral lesions

Fischer-Rasmussen & Jensen (2000)

20 27.0 (5.0) 20 27.0 (4.0) c N.R. N.R.

Fremery et al. (2000)

10 acute, 20 chronic

22.7(3.2) acute 28.4 (4.4) chronic

20 26.4 (4.8) p 6.3 (3.0) and 12.4 (3.7) months

12 meniscus lesions

Adachi et al. (2002)

29 median 27 (N.R.)

c median 8 (N.R.) months

N.R.

Katayama et al. (2004)

32 25.6 (N.R) c N.R. 7 meniscus lesions

Roberts et al. (2004)

54 28 (N.R.) c 2.7 (2.7) years 39 meniscus, 7 MCL and 7 chondral lesions

Ageberg et al. (2005)

36 (35 analyzed)

26 (5.0) c 3.8 (3.0) years N.R.

Roberts et al. (2007)

36 26 (5.4) c 3.8 (N.R.) years 19 meniscus, 6 MCL and 5 chondral lesions

Ageberg and Friden (2008)

67 (56 analyzed)

43 (8) 28 42 (9) c 15 (1.4) years 31 meniscus, 25 MCL, 11 chondral lesions

Lee et al. (2009)

12 (10 analyzed)

23.1 (1.8) 12.8 (3.9) months no

Muaidi et al. (2009)

20 30.4 (1.4) 20 29.5 (1.8) c n=20 5 weeks, n=1 10 weeks, n=1 7 months, n=1 5 years

13 injuries, mostly meniscus

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

51

Table 3. Demographics of subjects. (Continued)

Author n ACL Age (SD) n C Age

(SD) Design Time from injury (SD) Additional injury

ACL-R

Harter et al. (1992)

48 27.6 (6.9) - - c 4.1 (1.7) years N.R.

Co et al. (1993)

10 27 (N.R.) 10 24 (N.R.) c 31.6 (N.R.) months

8 meniscus and 2 MCL lesions

MacDonald (1996)

16 26.1 (N.R.) 6 30 (N.R.) c 27.5 (N.R) months

N.R.

Risberg (1999)

20 35 (N.R.) 10 33 (N.R.) c 24 (N.R.) 9 mensicus and 2 MCL lesions

Birmingham (2001)

30 27.2 (11.3) - - c 19.4 (14.5) months

N.R.

Reider (2003) 26 (21 analyzed)

25 (N.R) 26 25 (N.R.) p pre-op to 3 weeks, 6 weeks and 6 months (N.R.)

17 meniscus and 10 chondral lesions

Zhou et al.(2008)

36 26 (5.8) 13,0 26.4 (3.9) c 189 (11.2) days N.R.

Muaidi et al.(2009)

15 (3 months)14 (6 months)

30.4 (1.4) 20 29.5 (1.8) c 3 and 6 (N.R.) months

13 injuries, mostly meniscus

Abbreviations: ACL-D, Anterior Cruciate Ligament Deficient; ACL-R. Anterior Cruciate Ligament Reconstruction; n,number; C, Control subjects; c, cross sectional; MCL, Medial Collateral Ligament

The tests characteristics and correlation between proprioceptive tests and outcome measurements for the patients after ACLD and ACLR are presented in Table 4 and Table 5, for TTDPM and JPS, respectively.

Chapter 4

52

Tabl

e 4.

Res

ults

Pro

prio

cepti

on: T

hres

hold

to D

etec

t Pas

sive

Moti

on

Auth

or

Relia

bilit

y (*

)Sp

eed

°/s

Dire

ction

(°)

TTDP

M

ACL-

I (S

D)

TTDP

M

ACL-

U

(SD)

Diff

I-UES

TT

DPM

C

Left

(S

D)

TTDP

M

C Ri

ght

(SD)

Diff

C Le

ft-Ri

ght

Out

com

e m

easu

rem

ents

Corr

elati

on w

ith

TTDP

M (p

-val

ue)

ACL-

DCo

rrig

an e

t al.

(199

2)N

.R.

0,3

TE 3

5 an

d TF

35

mea

n 2.

6 (1

.8)

1.9

(1.2

)0,

70,

51.

2 (0

.4)

1.0

(0.5

)0,

2St

reng

th -

Isom

etric

H/Q

ratio

Invo

lved

leg

r=-0

.74

(<0.

01)

Uni

nvol

ved

leg

no

corr

elati

on (N

R)Co

ntro

ls r=

0.25

(0.4

1)W

right

et a

l. (1

995)

N.R

. 0,

5TE

40

3.2

(1.6

)3.

3 (1

.9)

0,1

-0,1

3.4

(1.5

)3.

5 (2

.1)

0,1

Laxi

ty -

KT-1

000

Diffe

renc

e in

volv

ed-

unin

volv

ed: r

=-0.

005

(N.R

.)Pa

tient

repo

rted

out

com

e -

Cinc

inna

ti Kn

ee R

ating

Diffe

renc

e in

volv

ed-

unin

volv

ed: r

=-0.

40

(N.R

.) Bo

rsa

et a

l. (1

997)

ICC

0.92

0,

5TE

15

0.9

(0.1

)0.

8 (0

.1)

0,1

2,5

Hop

test

- In

dex

singl

e le

g ho

p te

st d

istan

ceIn

volv

ed le

g TE

15

r=-0

.46

(< 0

.05)

TE 4

51.

1 (0

.1)

1.0

(0.1

)0,

11,

1In

volv

ed le

g TE

45

r=-0

.56

(< 0

.01)

TF 1

51.

1 (0

.1)

0.9

(0.1

)0,

21,

9In

volv

ed le

g TF

15

r=-0

.37

(N.R

.)TF

45

1.1

(0.1

)0.

9 (0

.1)

0,2

1,4

Invo

lved

leg

TF 4

5 r=

-0.4

7 (N

.R.)

Bors

a e

t al.

(199

8)IC

C 0.

92

0,5

inde

x sc

ore

65

(N.R

.)St

reng

th -

Isom

etric

Q

uadr

icep

sIn

volv

ed le

g r=

-0.2

9 (N

.R)

Hop

test

- In

dex

singl

e le

g ho

p te

st d

istan

ceIn

volv

ed le

g r=

-0.4

0 (N

.R.)

Bala

nce

- KAT

200

0In

volv

ed le

g r=

-0.0

7 (N

.R.)

Patie

nt

repo

rted

ou

tcom

e

Cinc

inna

ti Kn

ee

Ratin

gIn

volv

ed le

g r=

-0.3

4 (N

.R.)

Lysh

olm

Invo

lved

leg

r=-0

.19

(N.R

.)

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

53

Tabl

e 4.

Res

ults

Pro

prio

cepti

on: T

hres

hold

to D

etec

t Pas

sive

Moti

on (C

ontin

ued)

Auth

or

Relia

bilit

y (*

)Sp

eed

°/s

Dire

ction

(°)

TTDP

M

ACL-

I (S

D)

TTDP

M

ACL-

U

(SD)

Diff

I-UES

TT

DPM

C

Left

(S

D)

TTDP

M

C Ri

ght

(SD)

Diff

C Le

ft-Ri

ght

Out

com

e m

easu

rem

ents

Corr

elati

on w

ith

TTDP

M (p

-val

ue)

ACL-

DFr

iden

et a

l. (1

998)

CI 0

-0.3

80,

5TE

20

1.1

(0.9

)1.

1 (0

.9)

0,0

-0,1

0.8

(0.5

)Ho

p te

st -

Sin

gle

leg

hop

test

di

stan

ceIn

volv

ed le

g TE

20

r=-0

.42

(N.R

.)CI

0-0

.63

TE 4

0 0.

9 (0

.7)

1.4

(1.6

)-0

,5-0

,41.

0 (0

.6)

Invo

lved

leg

TE 4

0 r=

-0.5

8 (N

.R.)

CI 0

-0.2

5TF

20

0.8

(0.5

)1.

2 (0

.9)

-0,4

-0,5

1.1

(0.9

)In

volv

ed le

g TF

20

r=-0

.32

(N.R

.)CI

0-0

.13

TF 4

0 0.

8 (0

.7)

0.6

(0.2

)0,

20,

50.

7 (0

.4)

Invo

lved

leg

TF 4

0 r=

-0.4

6 (N

.R.)

Beyn

non

et a

l.(1

999)

Anal

ysis

varia

nce

0.57

0,5

TE45

and

TF

451.

5 (0

.7)

1.2

(0.5

)0,

30,

5La

xity

- KT

-100

0In

volv

ed le

g r=

0.15

(N

.R.)

Laxi

ty -

Pivo

t-shi

ftIn

volv

ed le

g r=

0.22

(N

.R.)

Frid

en e

t al.

(199

9)CI

0-0

.38

0,5

TE 2

0 1.

3 (1

.3)

1.0

(1.2

)0,

30,

2Pa

tient

repo

rted

out

com

e - S

ubje

ctive

Rati

ng k

nee

func

tion

(1-r

ecen

tly in

jure

d;

10=h

ealth

y w

ithou

t any

lim

itatio

n)

Invo

lved

leg

TE 2

0 at

8

mon

ths r

=0.6

1 (<

0.01

)CI

0-0

.63

TE 4

01.

2 (1

.0)

1.0

(0.7

)0,

50,

2In

volv

ed le

g TE

40

at 2

m

onth

s r=0

.64

(<0.

01)

CI 0

-0.2

5TF

20

2.3

(4.0

)1.

1 (1

.0)

0,8

0,4

Invo

lved

leg

TF 2

0 at

2

mon

ths r

=0.4

4 (<

0.01

)CI

0-0

.13

TF 4

0 1.

4 (2

.2)

0.8

(0.5

)0,

60,

4In

volv

ed le

g TF

40

at 1

m

onth

r=0.

65 (<

0.00

8)Ro

bert

s et a

l. (2

004)

CI 0

-0.6

3 0,

5in

dex

scor

e on

ly A

CL4.

5 (1

.1)

3.6

(1.1

)0,

90,

8La

xity

- La

chm

an

Prop

rioce

ptive

inde

x r=

0.33

(0.0

2)AC

L +

chon

dral

le

sion

15.2

(3

.1)

13.9

(0

.7)

1,2

0,6

Patie

nt

repo

rted

ou

tcom

e

Tegn

er

Subj

ectiv

e ra

ting

knee

func

tion

(1=r

ecen

tly

inju

red;

10

=hea

lthy

with

out a

ny

limita

tion)

Prop

riocp

etive

inde

x r=

-0.2

6 (0

.06)

Prop

riocp

etive

inde

x r=

-0.3

5 (<

0.01

)

Chapter 4

54

Tabl

e 4.

Res

ults

Pro

prio

cepti

on: T

hres

hold

to D

etec

t Pas

sive

Moti

on (C

ontin

ued)

Auth

or

Relia

bilit

y (*

)Sp

eed

°/s

Dire

ction

(°)

TTDP

M

ACL-

I (S

D)

TTDP

M

ACL-

U

(SD)

Diff

I-UES

TT

DPM

C

Left

(S

D)

TTDP

M

C Ri

ght

(SD)

Diff

C Le

ft-Ri

ght

Out

com

e m

easu

rem

ents

Corr

elati

on w

ith

TTDP

M (p

-val

ue)

ACL-

DAg

eber

g et

al.

(200

5)CI

0-0

.63

0,5

inde

x sc

ore

4.0

(2.0

)Ba

lanc

e M

ovem

ents

ex

eedi

ng 1

0mm

m

ean

of c

ente

r of

pre

ssur

e

Prop

rioce

ptive

inde

x r=

0.41

(0.8

1)

Spee

d of

m

ovem

ent

cent

er o

f pr

essu

re

Prop

rioce

ptive

inde

x r=

-0.2

7 (0

.10)

Patie

nt

repo

rted

ou

tcom

e

VAS

Subj

ectiv

e Ra

ting

knee

fu

nctio

n (0

=

tota

l disa

bilit

y;

100

= go

od k

nee

func

tion

- as

prio

r to

inju

ry)

Prop

rioce

ptive

inde

x r=

-0.2

9 (0

.08)

Tegn

erPr

oprio

cepti

ve in

dex

r=-0

.36

(0.0

3)Ro

bert

s et a

l. (2

007)

CI 0

-0.6

3 0,

5in

dex

scor

e4.

1 (2

.2)

Hop

test

- Si

ngle

leg

hop

test

di

stan

cePr

oprio

cepti

ve in

dex

r=-0

.40

(0.0

14)

Patie

nt re

port

ed o

utco

me-

Su

bjec

tive

Ratin

g kn

ee

func

tion

(0 =

tota

l disa

bilit

y;

100

= go

od k

nee

func

tion

- as

prio

r to

inju

ry)

Prop

rioce

ptive

inde

x r=

-0.3

0 (0

.06)

Ageb

erg

and

Frid

en (2

008)

CI 0

-0.6

3 0,

5in

dex

scor

e3.

3 (3

.8)

2.3

(0.7

) St

reng

th -

Isok

ineti

c Q

uadr

icep

sPr

oprio

cepti

ve in

dex

r=0.

06 (0

.58)

Hop

test

- sin

gle

leg

hop

test

di

stan

cePr

oprio

cepti

ve in

dex

r=-0

.11

(0.3

2)Pa

tient

re

porte

dou

tcom

e

KOO

S Pa

inPr

oprio

cepti

ve in

dex

r=-0

.15

(0.1

7)

KOO

S Sy

mpt

oms

Prop

rioce

ptive

inde

x r=

-0.1

2 (0

.24)

KOO

S AD

LPr

oprio

cepti

ve in

dex

r=-0

.13

(0.2

3)

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

55

Tabl

e 4.

Res

ults

Pro

prio

cepti

on: T

hres

hold

to D

etec

t Pas

sive

Moti

on (C

ontin

ued)

Auth

or

Relia

bilit

y (*

)Sp

eed

°/s

Dire

ction

(°)

TTDP

M

ACL-

I (S

D)

TTDP

M

ACL-

U

(SD)

Diff

I-UES

TT

DPM

C

Left

(S

D)

TTDP

M

C Ri

ght

(SD)

Diff

C Le

ft-Ri

ght

Out

com

e m

easu

rem

ents

Corr

elati

on w

ith

TTDP

M (p

-val

ue)

ACL-

DAg

eber

g an

d Fr

iden

(200

8)CI

0-0

.63

0,5

inde

x sc

ore

3.3

(3.8

) 2.

3 (0

.7)

Patie

nt

repo

rted

ou

tcom

e

KOO

S Sp

ort

Prop

rioce

ptive

inde

x r=

-0.1

3 (0

.22)

KOO

S Q

ualit

y of

life

Prop

rioce

ptive

inde

x r=

-0.1

2 (0

.25)

Te

gner

Prop

rioce

ptive

inde

x r=

-0.1

8 (0

.08)

Lee

et a

l. (2

009)

N.R

.0,

5TE

45

and

TF 4

5 m

ean

3.8

(2.6

)2.

6 (2

.0)

0,8

0,5

Bala

nce

- Tilt

ang

le d

ynam

ic

bala

nce

Invo

lved

leg

r=0.

58

(0.0

4)U

ninv

olve

d le

g r=

0.58

(0

.05)

ACL-

RCo

et a

l. (19

93)

N.R

.0,

5TE

40

1.3

(0.8

)1.

2 (0

.4)

0,1

1.7

(0.8

)2.

0 (1

.0)

-0,3

Stre

ngth

- Is

okin

etic

Qua

dric

eps

Invo

lved

leg

no

corr

elati

on (N

.R.)

Gai

t - H

eel s

trik

e tr

ansie

ntIn

volv

ed le

g no

co

rrel

ation

(N.R

.)M

acDo

nald

et

al. (

1996

)N

.R.

0,5

TE 3

0-40

TF

30-4

0 m

ean

0.8

(0.2

)0.

7 (0

.2)

0,1

0,5

0.8

(0.1

)0.

8 (0

.1)

0,0

Laxi

ty -

KT-1

000

40N

Invo

lved

leg

no

corr

elati

on (N

.R.)

Patie

nt re

port

ed o

utco

me

- Pa

tient

satis

facti

on (g

rade

0 to

5,

with

5 re

pres

entin

g 10

0%

satis

fied)

Invo

lved

leg

no

corr

elati

on (N

.R.)

Risb

erg

et a

l. (1

999)

CI 0

-0.6

3 0,

5TE

15

TF 1

5 m

ean

1.1

(0.6

)1.

1 (0

.8)

0,0

0,1

1.6

(0.9

)1.

5 (0

.6)

0,1

Patie

nt

repo

rted

ou

tcom

e

Invo

lved

le

gU

ninv

olve

d le

g

KOO

S Pa

in0.

21

(N.R

.)0.

34 (N

.R.)

KOO

S Sy

mpt

oms

0.17

(N

.R.)

0.22

(N.R

.)

KOO

S AD

L0.

09

(N.R

.)0.

17 (N

.R.)

KOO

S Sp

ort

0.14

(N

.R.)

0.27

(N.R

.)

Chapter 4

56

Tabl

e 4.

Res

ults

Pro

prio

cepti

on: T

hres

hold

to D

etec

t Pas

sive

Moti

on (C

ontin

ued)

Auth

or

Relia

bilit

y (*

)Sp

eed

°/s

Dire

ction

(°)

TTDP

M

ACL-

I (S

D)

TTDP

M

ACL-

U

(SD)

Diff

I-UES

TT

DPM

C

Left

(S

D)

TTDP

M

C Ri

ght

(SD)

Diff

C Le

ft-Ri

ght

Out

com

e m

easu

rem

ents

Corr

elati

on w

ith

TTDP

M (p

-val

ue)

ACL-

RRi

sber

g e

t al.

(199

9)CI

0-0

.63

0,5

TE 1

5 TF

15

mea

n1.

1 (0

.6)

1.1

(0.8

)0,

00,

11.

6 (0

.9)

1.5

(0.6

)0,

1Pa

tient

re

port

ed

outc

ome

Invo

lved

le

gU

ninv

olve

d le

g

KOO

S Q

ualit

y of

life

0.33

(N

.R.)

0.32

(N.R

.)

Cinc

inna

ti Kn

ee

Ratin

g0.

21

(N.R

.)0.

34 (N

.R.)

Hop

test

Sing

le le

g ho

p te

st d

istan

ce0.

40

(N.R

.)0.

55 (N

.R.)

Stai

r hop

test

0.15

(N

.R.)

0.30

(N.R

.)

Laxi

ty -

KT-1

000

134N

0.03

(N

.R.)

0.12

(N.R

.)

Reid

er e

t al.

(200

3)AN

OVA

va

rianc

e co

mpo

nent

ana

lysis

r=

0.96

3TE

15

TF 1

5 m

ean

3 w

eeks

2.3

(N.R

.)1.

8 (N

.R.)

0,5

1.5

(N.R

.)La

xity

- KT

-200

0 40

NIn

volv

ed le

g no

co

rrel

ation

(N.R

.)6

wee

ks1.

8 (N

.R.)

1.9

(N.R

.)-0

,1

3 m

onth

s1.

6 N

.R.)

1.6

(N.R

.)0

Patie

nt re

port

ed o

utco

me

- Ly

shol

mIn

volv

ed le

g no

co

rrel

ation

(N.R

.)6

mon

ths

1.6

(N.R

.)1.

5 (N

.R.)

0,1

Abbr

evia

tions

: N.R

., N

ot R

epor

ted;

TE,

Tow

ards

Ext

ensio

n; T

F, To

war

ds F

lexi

on; 1

5, 2

0, 3

0, 3

5, 4

0, 4

5, st

art p

ositi

on fl

exio

n of

the

knee

; TTD

PM, T

hres

hold

to D

etec

t Pa

ssiv

e M

otion

; ACL

-I, A

CL-In

volv

ed k

nee;

ACL

-U, A

CL U

ninv

olve

d kn

ee; D

iff I-

U, D

iffer

ence

Invo

lved

-Uni

nvol

ved;

ES,

Effe

ct S

ize; C

, Con

trol

gro

up; D

iff C

Left

-Rig

ht,

Diffe

renc

e Co

ntro

l Left

-Rig

ht k

nee;

(*),

refe

renc

e; H

/Q, H

amst

ring/

Qua

dric

eps

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

57

Tabl

e 5.

Res

ults

Pro

prio

cepti

on: J

oint

Pos

ition

Sen

se

Auth

or

Relia

bilit

yTe

st

mod

e (°

/s)

Dire

ction

(°)

JPS

ACL-

I (SD

)JP

S AC

L-U

(S

D)

Diff

I-U

ESJP

S C

Left

(S

D)

JPS

C Ri

ght

(SD)

Diff C

Left-

Righ

tO

utco

me

mea

sure

men

tsCo

rrel

ation

with

JP

S (p

val

ue)

ACL-

D Co

rrig

an e

t al.

(199

2)N

.R.

RAP

35 to

ext

ensio

n an

d to

fle

xion

5.3

(2.4

)4.

9 (2

.4)

0,4

0,2

2.8

(1.1

)2.

5 (0

.9)

0,3

Stre

ngth

- H/

Q ra

tioCo

ntro

ls r=

-0.2

5 (0

.40)

Uni

nvol

ved

leg

no

corr

elati

on (N

.R.)

Invo

lved

leg

r=-0

.77

(<0.

01)

Frem

ery

et a

l. (1

998)

N.R

. RP

P (0

.5)

0-20

flex

ion

acut

e 5.8

(1.9

)

chro

nic

3.5

(1.5

)

1.9

(0.5

)2.

1 (0

.7)

-0,2

Laxi

ty -

KT-1

000

max

forc

e in

30°

flex

ion

Invo

lved

leg

r= 0

.21

(N.R

.)

80-1

00 fl

exio

n8.

1 (2

.5)

2.2

(0.7

)2.

3 (0

.8)

-0,1

Patie

nt re

port

ed o

utco

me

- Pati

ent s

atisf

actio

nIn

volv

ed le

g r=

0.76

(N.R

.)Pa

tient

repo

rted

out

com

e - L

ysho

lmIn

volv

ed le

g r=

0.6

(N.R

.)Fi

sche

r-Ra

smus

sen

&

Jens

en (2

000)

N.R

. RA

P0

3.1

(1.0

)3.

1 (0

.9)

0,0

0,0

3.1

(1.1

)3.

2 (1

.0)

-0,1

Patie

nt re

port

ed o

utco

me

- ass

essm

ent p

erfo

rman

ce

(sco

re 0

-3)

Invo

lved

leg

rs=0

.6 (<

0.05

)60

flex

ion

4.1

(1.2

)3.

1 (0

.8)

1,0

0,9

3.0

(1.1

)3.

1 (1

.2)

-0,1

Kata

yam

a et

al

. (20

04)

N.R

. RP

P (1

0)be

twee

n 5-

25 fl

exio

n5.

2 (1

.9)

3.6

(1.5

)1,

60,

9Ho

p te

sts

Verti

cal h

opU

ninv

olve

d le

g r=

-0.3

1 (N

.R.)

Invo

lved

leg

r=-

0.33

(N.R

.)Si

ngle

leg

hop

dist

ance

Uni

nvol

ved

leg

r=-0

.20

(N.R

.)In

volv

ed le

g r=

-0.5

0 (<

0.00

1)Le

e et

al.

(200

9)N

.R.

RPP

(0.5

)45

to 0

ext

ensio

n45

to 9

0 fle

xion

4.6

(1.7

)3.

5 (1

.3)

0,9

0,7

Bala

nce

- Tilt

ang

le

dyna

mic

bal

ance

Invo

lved

leg

r=0.

024

(0.9

47)

Uni

nvol

ved

leg

r=0.

13 (0

.723

)

Chapter 4

58

Tabl

e 5.

Res

ults

Pro

prio

cepti

on: J

oint

Pos

ition

Sen

se (C

ontin

ued)

Auth

or

Relia

bilit

yTe

st

mod

e (°

/s)

Dire

ction

(°)

JPS

ACL-

I (SD

)JP

S AC

L-U

(S

D)

Diff

I-U

ESJP

S C

Left

(S

D)

JPS

C Ri

ght

(SD)

Diff C

Left-

Righ

tO

utco

me

mea

sure

men

tsCo

rrel

ation

with

JP

S (p

val

ue)

ACL-

D

Mua

idi e

t al.

(200

9)IC

C=0.

6RA

P0

to 1

5, 1

6.5,

18,

19.

5 IR

0 to

20

, 21.

5, 2

3, 2

4.5

ER

1.6

(0.1

)1.

5 (0

.1)

0,1

0,8

Laxi

ty -

pivo

t shi

ftIn

volv

ed le

g no

cor

rela

tion

(>0.

50)

Laxi

ty -

KT-1

000

max

forc

eIn

volv

ed le

g r=

0.35

(0.2

05)

Uni

nvol

ved

leg

r=0.

09 (0

.762

)Ho

p te

sts -

Sin

gle

leg

hop

dist

ance

In

volv

ed le

g r=

0.37

(0.1

91)

Uni

nvol

ved

leg

r=0.

10 (0

.724

)Pa

tient

repo

rted

out

com

e - I

KDC

2000

Invo

lved

leg

r=0.

42 (0

.115

)AC

L-R

Hart

er e

t al.

(199

2)N

.R.

RAP

15 fl

exio

n5.

6 (4

.1)

4.7

(3.9

)0,

90,

2La

xity

- KT

-100

0 90

NIn

volv

ed le

g r=

-0.2

2 (0

.13)

20 fl

exio

n5.

9 (4

.8)

5.6

(3.9

)0,

30,

1La

xity

- Pi

vot S

hift

Invo

lved

leg

r=0.

15 (0

.16)

25 fl

exio

n5.

0 (4

.0)

4.4

(4.0

)0,

60,

2La

xity

- Sl

ocum

Invo

lved

leg

r=-0

.13

(0.1

8)30

flex

ion

4.7

(4.7

)5.

3 (4

.1)

-0,6

-0,1

35 fl

exio

n5.

4 (4

.3)

5.4

(2.7

)0,

00,

0Bi

rmin

gham

(2

001)

N.R

.RA

Pbe

twee

n 30

-60

flexi

on3.

5 (1

.7)

Bala

nce

- On

firm

pl

atfor

m/e

yes o

pen

Invo

lved

leg

r=0.

00-0

.19

(0.3

2)Ba

lanc

e - O

n fo

am/e

yes

clos

edIn

volv

ed le

g r=

0.14

(>0.

50)

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

59

Tabl

e 5.

Res

ults

Pro

prio

cepti

on: J

oint

Pos

ition

Sen

se (C

ontin

ued)

Auth

or

Relia

bilit

yTe

st

mod

e (°

/s)

Dire

ction

(°)

JPS

ACL-

I (SD

)JP

S AC

L-U

(S

D)

Diff

I-U

ESJP

S C

Left

(S

D)

JPS

C Ri

ght

(SD)

Diff C

Left-

Righ

tO

utco

me

mea

sure

men

tsCo

rrel

ation

with

JP

S (p

val

ue)

ACL-

R

Zhou

et a

l. (2

008)

N.R

.RP

P (2

)0

to fl

exio

n5.

6 (2

.6)

4.3

(1.1

)St

reng

th -

Isok

ineti

c st

reng

thIn

volv

ed le

g r=

-0.4

1 (<

0.05

)St

reng

th -

Pre-

surg

ical

H/

Q p

eak

torq

ueIn

volv

ed le

g no

cor

rela

tion

(0.1

52)

Mua

idi e

t al.

(200

9)IC

C=0.

6RA

P0

to 1

5, 1

6.5,

18

, 19.

5 IR

0

to 2

0, 2

1.5,

23

, 24.

5 ER

3 mon

ths

1.3

(0.1

) 1.

4 (0.

1)

-0,1

-0.4

to

-0

.7

Patie

nt re

port

ed o

utco

me

- Cin

cinn

ati sp

ort a

ctivi

ty

ratin

g

Invo

lved

leg

(3

mo)

r=0.

63 (0

.021

)IC

C=0.

6RA

P6

mon

ths

1.3

(0.1

)1.

3 (0

.1)

0,0

Invo

lved

leg

(6 m

o) r=

0.22

(0

.44)

Patie

nt re

port

ed o

utco

me

- IKD

C 20

00

Invo

lved

leg

(3 m

o) r=

0.23

(0

.408

)In

volv

ed le

g (6

mo)

r=0.

05

(0.8

67)

Abbr

evia

tions

: N.R

., N

ot R

epor

ted;

RAP

, Rep

ositi

on A

ctive

Pos

ition

; RPP

, Rep

ositi

on P

assiv

e Po

sition

; 0, 5

, 15,

20,

25,

30,

35,

45,

60

star

t pos

ition

flex

ion

of th

e kn

ee;

IR, I

nter

nal R

otati

on; E

R, E

xter

nal R

otati

on; A

CL-I,

ACL

-Invo

lved

kne

e; A

CL-U

, ACL

Uni

nvol

ved

knee

; Diff

I-U,

Diff

eren

ce In

volv

ed-U

ninv

olve

d; E

S, E

ffect

Size

; C, C

ontr

ol

grou

p; D

iff C

Left

-Rig

ht, D

iffer

ence

Con

trol

Left

-Rig

ht k

nee;

H/Q

, Ham

strin

g/Q

uadr

icep

s

Chapter 4

60

The number of patients ranged between nine to 56 across all studies. In 12 studies, healthy controls were examined and compared to the patients.8,28,32,33,38-40,43-47 In most studies that examined TTDPM, tests speeds were 0.5°/sec, while two studies used speeds of 0.3°/sec and 3°/sec.33,47 JPS was tested in five studies with RAP28,30,33,35,39 and four studies measured RPP.36,37,44,46 The range of motion in which the knee was tested ranged between 15° and 45° flexion for TTDPM and between 0° and 100° flexion for JPS. Most studies reported a deficit for the involved ACLD or ACLR knee in comparison to the uninvolved leg. Mean deficits in TTDPM for the involved leg in patients after ACLD were 0.4 ± 0.4 and 0.2 ± 0.2° in patients after ACLR. A lower (better) TTDPM in ACLD patients for the involved leg compared to the uninvolved leg ranged between 0.1° to 0.5° in some test positions.34,44 One study found a lower TTDPM of 0.1° in the involved leg compared to the uninvolved leg six weeks after ACLR.47 The mean deficit for JPS in patients after ACLD was 0.8° ± 0.6 and 0.5° ± 0.4 in patients after ACLR. In two studies examining JPS in ACLR, lower values were found in the involved leg compared to the uninvolved leg (0.1° to 0.6°) in some of test positions.35,39 The mean ES was 0.4 ± 0.6. In healthy controls, the mean differences for TTDPM between the left and right leg were 0.1 ± 0.1°.33,38,40,43 In two studies mean results for TTDPM for left and right leg were combined to a value of 0.9° ± 0.2 34 and 1.5° (SD not reported)47 with the statement that there was no significant difference between the two legs. The mean difference between right and left leg in healthy controls for JPS was 0.1 ± 0.1°.28,33,46 Two studies reported only values for one leg in the control group and involved leg without side to side comparison.44,47

StrengthA correlation between proprioception and quadriceps strength was calculated in five studies.26,32,33,44,45 In two studies isometric strength26,33 was tested whereas three studies examined isokinetic strength.32,44,45 The two papers on isometric strength showed a good correlation with hamstring/quadriceps ratio and JPS (r = -0.74, p < 0.01)33 and a low correlation with isometric quadriceps strength and TTDPM (r = -0.29, p = N.R.) respectively.26 The three studies on isokinetic quadriceps strength found no correlation with TTDPM although p values were not provided,32 the second found no correlation (r = 0.06, p = 0.58),45 whereas for JPS a low correlation (r = -0.41, p < 0.05)44 was reported in the third.

GaitOne study reported no correlation between TTDPM and vertical ground reaction force at heel strike, although a statistical analysis of the data was not presented.32

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

61

LaxitySeven of the 10 studies found either no35,40,43,46,48 or a low39,42 correlation between proprioception and laxity. However, statistical significance was only achieved in one study with a low correlation (r = 0.33, p = 0.02)42 whereas in two studies the correlations were not significant.35,39 Four studies did not report the p-values.40,43,46,48 Three studies reported a non-significant correlation although data were not provided.25,38,47 Two of the principal authors of these studies25,38 responded to request to provide the data but stated that data was no longer available, while the other author did not respond.47

Hop testsOf the seven studies examining the correlation between proprioception and hop tests, one found no correlation (r = -0.11, p = N.R.),45 four a generally low 26,34,39,40 and two moderate correlations.31,36 Borsa et al. reported on the same cohort in two separate studies, but used different calculations of proprioceptive deficits, which resulted in a low correlation (no p-value) in one study26 and a moderate correlation in the other.31 A moderate correlation was found for TTDPM only at 40° of flexion while all other test positions demonstrated low correlations (no p-values reported).49

BalanceOf the four studies26,29,30,37 that examined balance, one study found a moderate correlation with proprioception (r = 0.58, p = 0.04).37 In the reaming three studies low to no correlations (r= 0.00 to 0.41) were found.26,29,30 The study that found a moderate correlation with TTDPM, did not find a correlation when examining JPS in the same patient population (r = 0.024, p = 0.947).37

Patient-reported outcomesCorrelation between proprioception and patient reported outcomes was examined in 15 studies. In four studies the correlation ranged between none and low for KOOS or Cincinnati score.26,40,43,45 The fifth study found a moderate correlation between proprioception and Cincinnati score at three months after ACLR (r = 0.63, p = 0.021) whereas at six months no correlation was observed (r = 0.22, p = 0.44).39 At three months there was no correlation with IKDC (r = 0.23, p = 0.408) and changed to a low correlation at six months (r = 0.44, p = 0.807). In three studies the correlation between proprioception and Lysholm was examined and found no correlation (r = -0.19, p = N.R.),26,47 or a moderate correlation (r = 0.6, p = N.R.)28 No correlation was found for Tegner score (r ranging from -0.18 to -0.36 and p ranging from 0.03 to 0.08).29,42,45 Four studies used a VAS score for subjective knee rating and found in general low

Chapter 4

62

correlations.8,29,41,42 The remaining three studies used patient satisfaction or performance rating questionnaires.28,38,46 No studies were found in which objective scores were examined.

D I S C U S S I O N

In general, low to moderate correlations between proprioception as measured with TTDPM and JPS and strength, hop tests and balance in ACLD or ACLR were found. No correlations were found between proprioception and laxity except for one study with a low correlation. The correlation with patient reported outcomes was in general not evident.

Methodological qualityA modified version of the Cochrane Methods Group on Screening and Diagnostic Tests (CM) methodology was used to assess the methodological quality.19 The mean methodology quality score was 8 ± 2 on the modified CM scoring checklist. Common flaws in methodological design were lack of reliability testing, incomplete statistical data, poor description of time since injury, in- and exclusion criteria of patients and their demographic data. All studies had a low level of evidence on the Oxford Center for Evidence-based Medicine Levels of Evidence. A maximum of five points could be scored on this item, but no study scored more than one point, due to the fact that no reference test was presented. Specific checklists for the current topic of interest are not available to the knowledge of the authors. It is recognized that this modified scoring system is arbitrary. However, the authors felt that weighing the included studies scoring was necessary to compare across studies. To add insight relative to the strength of the relationship between the variables of interest, ES was also calculated. The mean ES was 0.4 ± 0.6 and can be considered small.20

Outcome measurementsStrengthMuscle strength can be considered an important factor in maintaining joint stability. Joint stability can be defined as effectively resisting joint displacements and accomplished through a relationship between static and dynamic components. Static stability is measured through clinical joint stress testing in order to evaluate the integrity of the ligamentous structures and is not synonymous with functional stability. If static stability is compromised, such as with an ACL injury, compensation by dynamic components may become important in order to maintain functional stability of the

Proprioceptive Deficits after ACL Injury. Are they Clinically Relevant?

Chapter

4

63

knee. The dynamic components reflect the unconscious activation of the muscles in preparation for and in response to joint loading for the purpose of maintaining functional stability.50

The contention is that injury of the ACL results in altered proprioceptive input and subsequently leads to functional instability.51 The sensorimotor system involves the mechanisms responsible for the acquisition of a sensory stimulus along with transmission of the signal via afferent pathways to the Central Nervous System (CNS). At the CNS, the signal is processed by the various centers of the motor cortex and results in a motor response, which is required for maintenance of joint stability. The somatosensory system encompasses all of the mechanoreceptive, thermoreceptive and nociceptive information gathered from the periphery.50 Hence, proprioception is a sub-component of the somatosensory system and involves the acquisition of stimuli by articular, cutaneous and muscular and tendinous receptors. Therefore, proprioception involves only the afferent pathway of sensory information and is not involved in the motor response.50 This may explain why four of the five studies in this review found either no or a low correlation between strength and proprioception. Although, the authors of this review do not refute the importance of strength in generating sufficient functional stability, the relationship of strength with proprioception was not convincing.

LaxityNine of the 10 studies found no correlation between proprioception and laxity.25,35,38,40,42,43,46-48 except a low correlation in one study.39 Roberts et al. speculated that a proprioceptive deficit leads to an increase in laxity as a result of giving way episodes.42 A ligament-muscle reflex stimulating alpha and/or gamma motor neuron pathway has been reported52 and theoretically following ACL injury this ligament-muscle reflex is altered. The theory may lead to the assumption ACLR should therefore improve proprioception. Interestingly, the studies that examined patients after ACLR included in this review did not find a correlation with laxity and proprioception.35,38,40,47 Pre-operative baseline data was only presented in one study that showed improvement of proprioception after ACLR, yet no correlation with laxity could be established.47 The debate regarding the cause and effect relationship between laxity and proprioception may be fueled by the fact that a lack of significant relationship between laxity and functional stability has been demonstrated in ACLD.53 It is believed that proprioceptive deficits after ACL injury are caused by loss of mechanoreceptors located in the ACL.32,33 This seems plausible, however critical discussion points can be raised. First, there is the issue of validity. Although it is commonly accepted that proprioception is assessed by JPS and TTDPM, no golden reference test has been presented thus far that would support this assumption. Pincivero et al were one of the first to raise critical concerns

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pertaining the validity of current proprioception test methods.16,54 JPS and TTDPM do not differentiate between mechanoreceptors from the ACL and those arising from other mechanoreceptors in and around the knee joint.55 Secondly, it has recently been demonstrated that besides the afferent information from mechanoreceptors, the CNS can also contribute to JPS even when the CNS is deprived of peripheral afferent input. This illustrates a far more complex system than the contention that only peripheral information is essential.56 The CNS may play a more important role after ACL injury than previously thought. This can be exemplified by the existence of two distinct groups of patients after ACLD, the copers and non-copers. Both have an injury to the ACL, but only the non-copers experience instability. Better proprioception has been reported in non-copers versus copers.57 Interestingly, copers had altered somatosensory evoked potentials compared to non-copers, which may indicate that central somatosensory changes are the critical elements in development of an effective strategy to the stabilize the ACLD knee and not proprioception.57 It seems plausible that efficient CNS plasticity allows copers to maintain high athletic activity without instability of the knee whereas non-copers may lack this compensatory mechanism.58 Thirdly, the fact that proprioception is still altered after ACLR is often related to the fact that the graft does not contain receptors. This has recently been challenged, as reinnervation of the graft occurred as early as three months following ACLR.10 Lee and co-workers recently found a positive relationship between TTDPM and knee function at three months but not at six months post-surgery, highlighting the difficulty of interpreting the differences reported.37 Proprioceptive deficits persist after ACLR,12,38 however, baseline data is required to substantiate these claims. Only two studies included in this review provided baseline data which indicated that proprioception improves slightly after ACLR.46,47 The changes were relatively small and the authors of this review question their clinical relevance.

Hop testsIn general no or a low correlation between proprioception and hop tests was found in five studies26,39,40,45,49 and a moderate correlation in two studies.31,36 Six studies reported on ACLD and the remaining one study on ACLR.40 Borsa et al. reported on the same patients in two separate studies, but used different calculations of proprioceptive deficits, which resulted in low correlation in one study26 and a moderate correlation respectively in the other.31 Friden et al. reported generally low correlations between hop tests and TTDPM, except at 40° of flexion which showed a moderate correlation.49 In summary, the results are inconsistent and the correlation between hop tests and proprioception can not be established from the available data.

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BalanceThree studies found no correlation between proprioception and balance.26,29,30 The fourth study found a moderate correlation with TTDPM, but no correlation with JPS.37 There appears to be no correlation present between proprioception and balance in ACLD. Balance deficits that persist up to two years after ACLR are thought to be related to proprioceptive deficits.59 However, proprioception in this context continuous to be a frequent misused term. Balance has been incorrectly used synonymously with proprioception.50 It is known that balance exercises may improve outcome after ACLD.15 However, clear definitions are needed. Balance is defined as when postural equilibrium during all motor activities is achieved.60 With respect to balance, pertinent afferent information arises from vestibular, visual, and somatosensory sources. The afferent information gathered from these three sources must be integrated and processed to determine the necessary motor commands. The motor commands are then executed by muscles along the entire kinetic chain. Hence, it seems reasonable to conclude that the resultant outcome of exercises should be stated in exactly those terms such as improvement of balance, and not as improvement of proprioception.61 Hypothetically, skill training may allow a patient to improve the probability of detecting knee motion. The question remains if this would have any clinical relevance in terms of improved knee function or reduction of knee injury. It may be that the patient has improved the ability to respond to the standard cues provided by the current tests of proprioception by improved cognitive awareness and not by increased mechanoreceptor gain of the knee.

Patient reported outcome The current validated patient outcome such as KOOS, IKDC or Cincinnati62-64 were only presented in five studies.26,39,40,43,45 Four studies found no or a low correlation between proprioception and KOOS and or Cincinnati score, whereas one study reported a moderate correlation at three months after surgery.39 Interestingly, this changed to no correlation at six months after surgery. The IKDC had a low correlation six months after surgery.39 Therefore, the correlation between proprioception and patient reported outcome scores cannot be judged with certainty. Roberts et al. have noted larger proprioceptive deficits in symptomatic patients versus asymptomatic patients, although the Tegner scores were not different between both groups.11 Deficits are reportedly higher in patients with a cartilage and/or meniscus injury in addition to an ACL injury.49 However, there was no adverse effect on the Tegner score. The authors of this review recommend the use of validated patient outcome questionnaires for future research to provide accepted evaluation tools for comparison of studies.

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Clinical relevance of proprioceptive deficitsThe mean reported proprioceptive deficits for TTDPM and JPS were small in patients with a mean deficit for the involved leg of respectively 0.4° and 0.8° for ACLD and 0.2° and 0.5° for ACLR. The mean side to side differences in healthy subjects were 0.1° for TTDPM and 0.1° for JPS measurements. Therefore, even in comparison to healthy subjects, the differences are small and do not likely represent any clinical relevance. For example, one may ask if a mean proprioceptive deficit of 0.4° for TTDPM and 0.8° for JPS could discern between non-copers and copers after ACLD. Conversely, given the lack of reliability measurements in more than half of all included studies and the small differences observed, which likely fall within the range of measurement error, we view these differences as not clinically relevant. Jensen et al. examined proprioception between copers and non-copers and found no difference between both groups.65 Bilateral deficits in proprioception were reported to exist after ACL injury, in which case use of the uninvolved leg as an internal control might result in underestimation of the proprioceptive deficit.66 Patients after ACLD may have had a proprioceptive deficit prior to injury, which predisposed them to this injury. Scientific evidence to substantiate this claim is not available to the best knowledge of the authors. The use of passive tests for assessment of proprioception sense can be challenged. Under normal circumstances, the sensorimotor system gathers information from an active musculoskeletal system. In addition, there may not be a sound physiological rationale to justify using these extremely slow rates of knee displacement of 0.5°/sec as used in most studies. The detection of movement at these rates may not truly assess proprioception as it relates to its functional activities. From this review, it is now possible to evaluate the clinical relevance of reported proprioceptive deficits after ACL injury. However, there are some limitations associated with this review. This review only included studies in English, German and Dutch and could potentially cause language bias. Nonetheless, only four studies were excluded on language restrictions, indicating that outcome would not be considerably different if these would have been included. Only the two most commonly used measurement techniques to quantify proprioception were included. Proprioception assessed by TTDPM has been found to be more repeatable and precise than JPS, and other methods of assessing proprioception have even lower accuracy.18 It is recognized that the modified scoring system may be controversial. For instance, weighing of the items in the modified scoring system is arbitrary. This has to be taken into consideration when interpreting the results. A formal meta-analysis was not feasible due the heterogeneous data reported in the included studies.

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C O N C L U S I O N A N D F U T U R E D I R E C T I O N S

Although, proprioception has been examined thoroughly after injury of the ACL, this review indicates that proprioception testing to date has in general only a low to moderate correlation with function after ACL injury. However, it should be noted that the methodological quality of included studies was in general not high, which may indicate that higher quality studies, as well as newer, more accurate and precise methodologies, may change the conclusions as drawn from the current review. In light of the increasing rate of ACL injuries, as well as relative high recurrent injury rate after ACLR, the authors advise on development of new tests to determine the relevant role of the sensorimotor system. These tests should ideally be used as screening test for primary and secondary prevention of ACL injury.

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R E F E R E N C E S1. Spindler KP, Wright RW. Anterior Cruciate Ligament Tear. New Engl J Med. 2008;359(20):8p.

2. Hinterwimmer S, Engelschalk M, Sauerland S, Eitel F, Mutschler W. [Operative or conservative treatment of anterior cruciate ligament rupture: a systematic review of the literature]. Unfallchirurg. 2003;106(5):374-379.

3. Biau DJ, Tournoux C, Katsahian S, Schranz P, Nizard R. ACL reconstruction: a meta-analysis of functional scores. Clin Orthop Relat Res. 2007;458:180-187.

4. Kvist J, Ek A, Sporrstedt K, Good L. Fear of re-injury: a hindrance for returning to sports after anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2005;13(5):393-397.

5. Spindler KP, Kuhn JE, Freedman KB, Matthews CE, Dittus RS, Harrell FE. Anterior cruciate ligament reconstruction autograft choice: bone-tendon-bone versus hamstring: does it really matter? A systematic review. Am J Sports Med. 2004;32(8):1986-1995.

6. Shelbourne KD, Gray T, Haro M. Incidence of subsequent injury to either knee within 5 years after anterior cruciate ligament reconstruction with patellar tendon autograft. Am J Sports Med. 2009;37(2):246-251.

7. Oiestad BE, Engebretsen L, Storheim K, Risberg MA. Knee osteoarthritis after anterior cruciate ligament injury: a systematic review. Am J Sports Med. 2009;37(7):1434-1443.

8. Friden T, Roberts D, Zatterstrom R, Lindstrand A, Moritz U. Proprioceptive defects after an anterior cruciate ligament rupture - the relation to associated anatomical lesions and subjective knee function. Knee Surg Sports Traumatol Arthrosc. 1999;7(4):226-231.

9. Barrett DS. Proprioception and function after anterior cruciate reconstruction. J Bone Joint Surg Br. Sep 1991;73(5):833-837.

10. Ochi M, Iwasa J, Uchio Y, Adachi N, Sumen Y. The regeneration of sensory neurones in the reconstruction of the anterior cruciate ligament. J Bone Joint Surg Br. Sep 1999;81(5):902-906.

11. Roberts D, Friden T, Zatterstrom R, Lindstrand A, Moritz U. Proprioception in people with anterior cruciate ligament-deficient knees: comparison of symptomatic and asymptomatic patients. J Orthop Sports Phys Ther. Oct 1999;29(10):587-594.

12. Bonfim TR, Jansen Paccola CA, Barela JA. Proprioceptive and behavior impairments in individuals with anterior cruciate ligament reconstructed knees. Arch Phys Med Rehabil. Aug 2003;84(8):1217-1223.

13. Jerosch J, Schaffer C, Prymka M. [Proprioceptive abilities of surgically and conservatively treated knee joints with injuries of the cruciate ligament]. Unfallchirurg. 1998;101(1):26-31.

14. Friden T, Roberts D, Ageberg E, Walden M, Zatterstrom R. Review of knee proprioception and the relation to extremity function after an anterior cruciate ligament rupture. J Orthop Sports Phys Ther. 2001;31(10):567-576.

15. Cooper RL, Taylor NF, Feller JA. A systematic review of the effect of proprioceptive and balance exercises on people with an injured or reconstructed anterior cruciate ligament. Res Sports Med. 2005;13(2):163-178.

16. Pincivero DM, Coelho A.J. Proprioceptive measures warrant scrutiny. Biomech. 2001(803):77-84.

17. Lephart SM RB, Fu FH. Introduction to the sensorimotor system. In: Lephart SM FF, ed. Proprioception and neuromuscular control in joint stability. Champaign, Illinois: Human Kinetic; 2000.

18. Beynnon BD RP, Konradsen L, Elmqvist L-G, Gottlieb D, Dirks M. Validation of techniques to measure knee proprioception. In: Lephart SM FF, ed. Proprioception and neuromuscular control in joint stability. Champaign, Illinois: Human Kinetics; 2000:127-138.

19. Deville WL, Buntinx F, Bouter LM, et al. Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol. 2002;2:9.

20. Cohen J. Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Lawrence Erlbaum Associates; 1988.

21. Al-Othman AA. Clinical measurement of proprioceptive function after anterior cruciate ligament reconstruction. Saudi Med J. 2004;25(2):195-197.

22. Bonfim TR, Paccola CAJ. Proprioception after anterior cruciate ligament reconstruction using auto and allograft patellar ligament. Revis Brasil Ortop. 2000;35(6):194-201.

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23. Ma YH, Cheng AL, Bai YH, et al. Effects of proprioception enhancement training on joint position sense after anterior cruciate ligament reconstruction. Chin J Clin Rehabil. 2005;9(10):16-17.

24. Mao J, Liu MJ. Flexor and extensor strength and proprioception reconstruction after knee cruciate ligament injury. Journal of Clin Rehabil Tiss Eng Res. 2008;12(37):7330-7333.

25. Adachi N, Ochi M, Uchio Y, Iwasa J, Ryoke K, Kuriwaka M. Mechanoreceptors in the anterior cruciate ligament contribute to the joint position sense. Acta Orthop Scand. 2002;73(3):330-334.

26. Borsa PA, Lephart SM, Irrgang JJ. Comparison of performance-based and patient-reported measures of function in anterior-cruciate-ligament-deficient individuals. J Orthop Sports Phys Ther. 1998;28(6):392-399.

27. Carter ND, Jenkinson TR, Wilson D, Jones DW, Torode AS. Joint position sense and rehabilitation in the anterior cruciate ligament deficient knee. Br J Sports Med. 1997;31(3):209-212.

28. Fischer-Rasmussen T, Jensen PE. Proprioceptive sensitivity and performance in anterior cruciate ligament-deficient knee joints. Scand J Med Sci Sports. 2000;10(2):85-89.

29. Ageberg E, Roberts D, Holmstrom E, Friden T. Balance in single-limb stance in patients with anterior cruciate ligament injury: relation to knee laxity, proprioception, muscle strength, and subjective function. Am J Sports Med. 2005;33(10):1527-1535.

30. Birmingham TB, Kramer JF, Kirkley A, Inglis JT, Spaulding SJ, Vandervoort AA. Knee bracing after ACL reconstruction: effects on postural control and proprioception. Med Sci Sports Exerc. 2001;33(8):1253-1258.

31. Borsa PA, Lephart SM, Irrgang JJ, Safran MR, Fu FH. The effects of joint position and direction of joint motion on proprioceptive sensibility in anterior cruciate ligament-deficient athletes. Am J Sports Med. 1997;25(3):336-340.

32. Co FH, Skinner HB, Cannon WD. Effect of reconstruction of the anterior cruciate ligament on proprioception of the knee and the heel strike transient. J Orthop Res. 1993;11(5):696-704.

33. Corrigan JP, Cashman WF, Brady MP. Proprioception in the cruciate deficient knee. J Bone Joint Surg Br. 1992;74(2):247-250.

34. Friden T, Roberts D, Movin T, Wredmark T. Function after anterior cruciate ligament injuries. Influence of visual control and proprioception. Acta Orthop Scand. 1998;69(6):590-594.

35. Harter RA, Osternig LR, Singer KM. Knee joint proprioception following anterior cruciate ligament reconstruction. J Sport Rehabil. 1992;1(2):103-110.

36. Katayama M, Higuchi H, Kimura M, et al. Proprioception and performance after anterior cruciate ligament rupture. Int Orthop. 2004;28(5):278-281.

37. Lee HM, Cheng CK, Liau JJ. Correlation between proprioception, muscle strength, knee laxity, and dynamic standing balance in patients with chronic anterior cruciate ligament deficiency. Knee. 2009;16(5):387-391.

38. MacDonald PB, Hedden D, Pacin O, Sutherland K. Proprioception in anterior cruciate ligament-deficient and reconstructed knees. Am J Sports Med. 1996;24(6):774-778.

39. Muaidi QI, Nicholson LL, Refshauge KM, Adams RD, Roe JP. Effect of anterior cruciate ligament injury and reconstruction on proprioceptive acuity of knee rotation in the transverse plane. Am J Sports Med. 2009;37(8):1618-1626.

40. Risberg MA, Beynnon BD, Peura GD, Uh BS. Proprioception after anterior cruciate ligament reconstruction with and without bracing. Knee Surg Sports Traumatol Arthrosc. 1999;7(5):303-309.

41. Roberts D, Ageberg E, Andersson G, Friden T. Clinical measurements of proprioception, muscle strength and laxity in relation to function in the ACL-injured knee. Knee Surg Sports Traumatol Arthrosc. 2007;15(1):9-16.

42. Roberts D, Andersson G, Friden T. Knee joint proprioception in ACL-deficient knees is related to cartilage injury, laxity and age: a retrospective study of 54 patients. Acta Orthop Scand. 2004;75(1):78-83.

43. Wright SA, Tearse DS, Brand RA, Gabel RH. Proprioception in the anteriorly unstable knee. Iowa Orthop J. 1995;15:156-161.

44. Zhou M-w, Gu L, Chen Y-p, et al. Factors affecting proprioceptive recovery after anterior cruciate ligament reconstruction. Chin Med J. 2008;121(22):2224-2228.

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45. Ageberg E, Friden T. Normalized motor function but impaired sensory function after unilateral non-reconstructed ACL injury: patients compared with uninjured controls. Knee Surg Sports Traumatol Arthrosc. 2008;16(5):449-456.

46. Fremerey RW, Lobenhoffer P, Born I, Tscherne H, Bosch U. [Can knee joint proprioception by reconstruction of the anterior cruciate ligament be restored? A prospective longitudinal study]. Unfallchirurg. 1998;101(9):697-703.

47. Reider B, Arcand MA, Diehl LH, et al. Proprioception of the knee before and after anterior cruciate ligament reconstruction. Arthroscopy. 2003;19(1):2-12.

48. Beynnon BD, Ryder SH, Konradsen L, Johnson RJ, Johnson K, Renstrom PA. The effect of anterior cruciate ligament trauma and bracing on knee proprioception. Am J Sports Med. 1999;27(2):150-155.

49. Friden T, Roberts D, Zatterstrom R, Lindstrand A, Moritz U. Proprioception in the nearly extended knee. Measurements of position and movement in healthy individuals and in symptomatic anterior cruciate ligament injured patients. Knee Surg Sports Traumatol Arthrosc. 1996;4(4):217-224.

50. Riemann BL, Lephart SM. The Sensorimotor System, Part I: The Physiologic Basis of Functional Joint Stability. J Athl Train. 2002;37(1):71-79.

51. Beard DJ, Dodd CA, Trundle HR, Simpson AH. Proprioception enhancement for anterior cruciate ligament deficiency. A prospective randomised trial of two physiotherapy regimes. J Bone Joint Surg Br. 1994;76(4):654-659.

52. Johansson H, Sjolander P, Sojka P. A sensory role for the cruciate ligaments. Clin Orthop Relat Res. 1991(268):161-178.

53. Snyder-Mackler L, Fitzgerald GK, Bartolozzi AR, 3rd, Ciccotti MG. The relationship between passive joint laxity and functional outcome after anterior cruciate ligament injury. Am J Sports Med. 1997;25(2):191-195.

54. Pincivero DM, Bachmeier B, Coelho AJ. The effects of joint angle and reliability on knee proprioception. Med Sci Sports Exerc. 2001;33(10):1708-1712.

55. Hogervorst T, Brand RA. Mechanoreceptors in joint function. J Bone Joint Surg Am. 1998;80(9):1365-1378.

56. Smith JL, Crawford M, Proske U, Taylor JL, Gandevia SC. Signals of motor command bias joint position sense in the presence of feedback from proprioceptors. J Appl Physiol. 2009;106(3):950-958.

57. Courtney C, Rine RM, Kroll P. Central somatosensory changes and altered muscle synergies in subjects with anterior cruciate ligament deficiency. Gait Posture. 2005;22(1):69-74.

58. Kapreli E, Athanasopoulos S. The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses. 2006;67(3):645-650.

59. Zouita Ben Moussa A, Zouita S, Dziri C, Ben Salah FZ. Single-leg assessment of postural stability and knee functional outcome two years after anterior cruciate ligament reconstruction. Ann Phys Rehabil Med. 2009;52(6):475-484.

60. Riemann BL. Is There a Link Between Chronic Ankle Instability and Postural Instability? J Athl Train. 2002;37(4):386-393.

61. Ashton-Miller JA, Wojtys EM, Huston LJ, Fry-Welch D. Can proprioception really be improved by exercises? Knee Surg Sports Traumatol Arthrosc. 2001;9(3):128-136.

62. Barber-Westin SD, Noyes FR, McCloskey JW. Rigorous statistical reliability, validity, and responsiveness testing of the Cincinnati knee rating system in 350 subjects with uninjured, injured, or anterior cruciate ligament-reconstructed knees. Am J Sports Med. 1999;27(4):402-416.

63. Irrgang JJ, Anderson AF, Boland AL, et al. Development and validation of the international knee documentation committee subjective knee form. Am J Sports Med. 2001;29(5):600-613.

64. Roos EM, Roos HP, Lohmander LS, Ekdahl C, Beynnon BD. Knee Injury and Osteoarthritis Outcome Score (KOOS) -development of a self-administered outcome measure. J Orthop Sports Phys Ther. 1998;28(2):88-96.

65. Jensen TO, Fischer-Rasmussen T, Kjaer M, Magnusson SP. Proprioception in poor- and well-functioning anterior cruciate ligament deficient patients. J Rehabil Med. 2002;34(3):141-149.

66. Jerosch J, Prymka M. Proprioception and joint stability. Knee Surg Sports Traumatol Arthrosc. 1996;4(3):171-179.

Chapter 5Movement Patterns of Patients Immersed in Virtual Reality after ACL Reconstruction

A. Gokeler, M. Bisschop, G.D. Myer, A. Benjaminse, P.U. Dijkstra, H.G. van Keeken, J.J.A.M. van Raaij, J.G.M. Burgerhof, E. Otten

Accepted Knee Surg Sports Traumatol Arthrosc 2014

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A B S T R A C T

Purpose: Despite ACL-reconstruction (ACLR), patients often show persistent asymmetric movements patterns during activities of daily living and sport specific tasks. It is conceivable that patients use an attentional focus that is directed to conscious control of the movements (internal focus) to avoid loading their involved leg. Virtual reality is a powerful tool for simulating aspects of the real world. The purpose of this study is to evaluate the influence of immersion in virtual reality environment on knee biomechanics in patients after ACLR. The patients were be embedded in a virtual reality setting in order to distract them from their conscious control of the knee. It is hypothesized that patients reach a more normalized movement pattern in a virtual reality environment compared to a non-virtual reality environment because it distracts them from their conscious motor control.Methods: Twenty athletes following ACLR and 20 healthy controls (CTRL) performed a step down task in both a non-virtual reality environment and in a virtual reality environment. Knee joint biomechanics were measured and analyzed during each single-leg landing. Results: A significant main effect was found for environment for knee flexion excursion (P = 0.031). Significant interactions differences were found between environment and groups for vertical ground reaction force (GRF) (P = 0.004), knee moment (P < 0.001), knee angle at peak GRF (P = 0.011) and knee flexion excursion (P = 0.032). In virtual reality environment knee biomechanics of patients after ACLR increased more than those of controls. Conclusion: Patients after ACLR immersed in virtual reality environment demonstrated knee joint biomechanics that approximate those of CTRL. The results of this study suggest that virtual reality environment distracts patients after ACLR from conscious motor control. The results of this study suggest that altered movement patterns after ACLR may be effectively targeted with novel motor learning techniques.

Key words: Anterior cruciate ligament; motor learning; external focus; knee biomechanics

Level of evidence: Diagnostic study, III

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I N T R O D U C T I O N

Between 250,000 – 300,000 anterior cruciate ligament (ACL) injuries occur in the United States per year1, and most athletes are advised to undergo ACL-reconstruction (ACLR) with the expectation that surgery will restore knee function and facilitate return to previous levels of activity.2 However, successful ACLR in terms of restoring the mechanical stability of the knee joint is not synonymous with restoration of normal knee function.3 After ACLR, altered movement patterns and neuromuscular impairments are consistently found during activities such as walking, running and jumping.4-12 Asymmetries in multidimensional knee biomechanics (kinematics and kinetics) during daily tasks as well as athletic activities are reported for up to five years after ACLR.4,13-19 Altered movement patterns after ACLR may be useful in the acute stage after surgery as the patient may choose to move the involved leg carefully to reduce pain or prevent instability. Theoretically, altered movement patterns should be time dependent if we accept the premise that movement has potential to be restored to normal levels during the course of rehabilitation after ACLR. Unfortunately, it was recently demonstrated that biomechanical deficits evidenced by reduced force generation and force absorption are independent of time after ACLR.20 There is a need to expand the current body of knowledge in understanding how and why altered movement patterns develop and can be reversed with rehabilitation following ACLR. Concepts of motor learning may help shrink this gap in knowledge. Motor learning is defined as the process of the person’s capability in acquiring motor skills with a permanent change.21,22

Effective motor control calls for an efficient information processing between the body, brain and environment (embodied cognition).23 The classical view is that cognitive control is necessary as a prerequisite before a subject reaches the stage during which movement control occurs more or less automatically.24 Based on this contention, during the early stages of motor re-learning, the execution of movement requires attention, so that there exists a dependency on cognitive control.24

Based on aforementioned, it may be plausible that patients after ACLR may utilize an increased attentional, cognitive focus on movement which inhibits the learning process of regaining normal movements. Researchers have defined an internal and external focus to describe attentional demands in motor learning and rehabilitation to (re-) acquire motor skills.25-30 Typically, feedback provided by clinicians during rehabilitation sessions refers to attention of body movements. The treating clinician may tell a patient who has an altered gait pattern after ACLR to extend the knee more during the stance phase. In the motor learning domain, this type of attentional focus is termed “internal focus”.31 Conversely, an external focus of attention is induced when a patient’s attention is directed towards the outcome or effects of the movement (e.g., “imagine to kick a ball”, to facilitate extension of the knee).

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Adopting an external focus has been shown to be more effective in motor learning because it directs the patient’s attention away from their own movements and shifts it towards the outcome of movements.21 A continued internal focus may be detrimental to motor learning as conscious control of movements interferes with automatic motor control processes that would “normally” regulate the movement.32 Patients who actively intervene in the control of their movements, i.e. using an internal focus, seem to constrain the motor system and degrade the natural movement. Such action results in decreased performance and altered movement patterns.30 Clinically, it appears that patients after ACLR utilize such an internal focus to constrain the movements of the knee joint although this strategy has not been previously evaluated or reported in the literature to the best of our knowledge. Therefore, the challenge is to develop experiments that might test these hypotheses. Virtual reality may be an appropriate tool because it allows for manipulation of visual and auditory feedback to reassure that all subjects are examined under the identical circumstances. In addition, with virtual reality it is possible to manipulate the environment that would be impractical or impossible to create in the real world.33 Kinematics of movements performed in a virtual reality environment are remarkably similar to those when acting in the real world.33 Virtual reality may also be employed in patients after ACLR to measure the changes in strategy they use as a result of a change in environmental embedding. This embedding may “distract” the patient after ACLR resulting in a change of the motor control due to a change in attention.34 The purpose of the current study was to evaluate the influence of immersion in virtual reality on movement patterns in patients after ACLR while performing a step down task. We hypothesized that virtual reality techniques aimed to alter attentional focus will increase knee flexion angle, knee moment and vertical ground reaction force in patients following ACLR.

M AT E R I A L A N D M E T H O D S

SubjectsWe recruited 20 patients after ACLR (10 males, 10 females) with a mean age of 23.5 ± 4.3 years from the Orthopaedic Surgery department of the Martini Hosptial, Groningen, the Netherlands. The patients after ACLR were all cleared to return to sports by their physical therapist and the orthopedic surgeon. Inclusion criteria for ACLR group were: 1) between the ages of 18-45, 2) < one year between injury and ACLR, 3) patient participated in rehabilitation program outlined by the hospital and 4) active in sports after surgery. Exclusion criteria were 1) swelling of the operated knee joint, 2) varus malalignment of the knee, 3) grade 3 injury of the collateral ligaments, 4) concomitant ligamentous injuries to the posterolateral corner, 5) > 50% base menisectomy, 6)

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traumatic cartilage injuries, 7) degenerative changes of the knee joint, 8) surgical procedures or injuries to the contralateral leg and 9) neurological and/or vestibular disease. Patients after ACLR were tested at a mean of 8.9 ± 2.3 months after surgery. The CTRL group included 20 healthy subjects (10 males and 10 females) with a mean age of 22.7 ± 2.3 years. The exclusion criteria for the CTRL group were as follows: 1) surgical procedures or injuries to the contralateral leg and 2) neurological and/or vestibular disease. The characteristics of all subjects are shown in Table 1.

Table 1. Demographic data of control and ACLR subjects, mean (± SD).

Control subjects ACLR subjects

Age (years) 22.7 ± 2.3 23.5 ± 4.3

Gender (n) male (10), female (10) male (10), female (10)

Mass (kg) 71.4 ± 10.7 75.2 ± 12.3

Height (cm) 178.9 ± 10.0 179.2 ± 8.4

Left leg length (cm) 93.5 ± 6.9 94.0 ± 5.9

Right leg length (cm) 93.4 ± 6.9 94.0 ± 5.9

Dominant lega (n) left (3), right (17) left (0), right (20)

Injured knee (n) - left (9), right (11)

Time since injury (months) - 18.1 ± 12.3

Time since surgery (months) - 8.9 ± 2.3

Hours sport per week (prior injury for ACLR subjects)

4.7 ± 2.6 6.8 ± 3.8

IKDC score* 97.6 ± 5.1 77.9 ± 12.9a Dominant leg was defined as the leg with which subject would kick a ball. * Significant difference between groups (p<0.001).

We designed our study based on continuous response variables from independent control and experimental subjects with one control(s) per experimental subject. Based on a similar study related to biomechanics during stair descent15 a minimum of nine study subjects per group was needed to reject the null hypothesis with 80% power and a Type I error probability at 0.05.

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Test protocolInstrumentationAll subjects wore their own athletic shoes during the test session. Prior to testing, each subject was fitted with 11 retroreflective markers of 14 mm in diameter (MotionCap, USA). The markers were placed on top of the head, spinous process Th7, midline PSIS and bilateral on greater trochanter, lateral epicondyle femur, lateral malleolus and base 5th metatarsal. Before each data collection session, the motion analysis system was calibrated to manufacturer recommendations. Each subject underwent motion analysis during a step down from a 20 cm high box onto two force plates (Bertec Corporation, Columbus, USA) of 40×60 cm that were embedded in the floor in front of the box. Twelve infrared cameras V8 Workstation 4.6 (VICON, Oxford, UK) were positioned in the Computer Assisted Rehabilitation Environment - CAREN lab (Motek Medical, Amsterdam, the Netherlands) that defined a capture volume (m3) with dimensions of 4.5 × 4 × 2.5 m. In addition, sorting of template based marker matching was obtained prior to each trial. The 3D marker positions recorded during the trials were captured by the Vicon motion analysis system (VICON, Oxford, UK). These data were transferred to DFlow (Motek Medical, Amsterdam, the Netherlands) at a sample rate of 120 Hz via a TCP-IP network.

Data collection The sequence of stepping down for patients was eight trials with the involved leg followed by eight trials for the uninvolved leg. CTRL first stepped down with the dominant leg, defined as the leg which they would kick a ball with, followed by the non-dominant leg. Other than instructions on when to step, the subjects were told to keep the arms across the chest to prevent occlusion of the hip markers. The step was deemed correct by the experimenter when the subject landed with one foot on the force plate.The experiment was divided in a non-virtual reality and a virtual reality environment condition which was custom developed for the purpose of this study. The non-virtual environment depicted a traffic light which changed from red to green projected on a grey 3.65×2.70 m screen. In comparison, the virtual reality environment was a traffic environment depicting a city street, with high buildings and a crosswalk with a pedestrian traffic light and cars projected on the screen passing from left to the right (Figure 1). We controlled for visual influences as patients were asked in both conditions to look at the same screen. In addition to visual input, stereo sound with common traffic noise was added to the virtual reality environment. In both environments, the traffic light was placed at the exact same spot and changed randomly from red to green between 15 – 25 seconds. The subjects were instructed to step down once the red light changed to green. For the virtual environment, all subjects received the instruction to pay attention

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to the oncoming traffic. All subjects stepped down first in non-virtual reality followed by the virtual reality environment. All subjects performed a total of 32 trials (eight trials for each leg per environment).

Figure 1. Subject in the virtual reality environment depicting a traffic scene with a crosswalk and a pedestrian traffic light. Upon switching the traffic light from red to green, the subject stepped down the box onto the force plate placed in front of the box.

Data processingData processing was performed with D-Flow (Motek, the Netherlands) and MATLAB version R2010a (The MathWorks, Inc., Natick, Massachusetts, USA). The raw data was processed with a zero lag filter with smooth cut-off in the frequency domain to avoid ringing with minimal jerk convolution filter of a bell shaped profile with the signal. A custom program was written to calculate the various biomechanical variables. The peak vertical ground reaction force (GRF) was calculated as the peak magnitude of the landing force normalized to body weight (N/BW). The peak internal knee extension moment was normalized to BW (Nm/BW). The knee angle was defined as the angle at peak GRF. Knee flexion excursion was the displacement of the knee (in degrees) in the sagittal plane and was calculated from the knee angle during initial foot contact (IC) to the largest flexion angle during stance phase. IC was defined when the vertical GRF exceeded 10N.

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Statistical analysisA generalized linear mixed model analysis in SPSS version 20 (SPSS, Inc., Chicago, USA) was applied to examine the influence of environment (virtual reality versus non-virtual reality) in the two subject groups. Data was analyzed with an ANOVA in the context of a linear mixed model because we did not have eight repeated measures for each individual. The involved leg of individuals in the ACLR group was compared to the non-dominant leg of individuals in the CTRL group which has been shown to accurately detect differences between groups.35 The dependent variables of interest were peak vertical GRF, maximum internal knee extension moment, knee angle at peak GRF and knee flexion excursion. Main effects of group (ACLR/CTRL) and environment, and their interaction were included in the model. Based on the Likelihood Ratio test, the interaction term was removed from the model if the P-value was larger than 0.05. The intercept was assigned to the non-dominant leg of the CTRL group. Statistical significance was established a priori at P < 0.05.

R E S U LT S

Significant interactions between environment and groups were found for the dependent variables GRF (P = 0.004), peak internal knee extension moment (P < 0.001), knee angle at peak GRF (P = 0.011) and knee flexion excursion (P = 0.032) (Table 2). This was demonstrated by significant differences for all measurements. The GRF was lower in the ACLR group in non-virtual reality (1.41 N/BW ± 0.32) compared to CTRL (1.52 N/BW ± 0.19) but increased when immersed in virtual reality (1.52 N/BW ± 0.35) with no change in the CTRL group. An increase in peak internal knee moment in virtual reality was also noted for the ACLR group (1.05 Nm/BW ± 0.48 to 1.20 Nm/BW ± 0.53). Interestingly, the CTRL showed a decrease (1.24 Nm/BW ± 0.60, 1.19 Nm/BW ± 0.56) in knee moment in virtual reality compared to non-virtual reality. Peak knee angle during non-virtual in the ACLR group (27.00° ± 8.72) increased marginally in virtual reality (28.13° ± 7.64) and decreased in the CTRL group (26.51° ± 7.62, 25.71° ± 7.38). The influence of virtual reality on knee flexion excursion was significantly different between groups, with the ACLR group demonstrating a very small increase (12.64° ± 4.82, 12.83° ± 4.05) compared with a decrease for CTRL (14.14° ± 5.94, 13.01° ± 4.86).

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Table 2. Results for the dependent biomechanical variables during non-virtual reality and virtual reality for the ACLR and CTRL group.

NVR VR NVR VR P value P value P value*

ACLR (mean ± SD)

ACLR(mean ± SD)

CTRL (mean ± SD)

CTRL(mean ± SD)

ACLR versus CTRL

Environ-ment

Interaction Group x Environment

Peak vertical GRF (N/BW)

1.41 ± 0.32

1.52 ± 0.35

1.52 ± 0.19

1.52 ± 0.17

0,816 0,737 0.004*

Peak internal knee extension moment (Nm/BW)

1.05 ± 0.48

1.20 ± 0.53

1.24 ± 0.60

1.19 ± 0.56

0,847 0,388 <0.001*

Knee angle at peak GRF (degrees)

27.00 ± 8.72

28.13 ± 7.64

26.51 ± 7.62

25.71 ± 7.38

0,268 0,466 0.011*

Knee flexion excur-sion (degrees)

12.64 ± 4.82

12.83 ± 4.05

14.14 ± 5.94

13.01 ± 4.86

0,875 0.031* 0.032*

Abbreviations: NVR, non-virtual reality; VR, virtual reality; ACLR, involved leg ACL group; CTRL, non-dominant leg of the CTRL group; GRF, ground reaction force; BW, body weight; SD, standard deviation; * denotes statistical significance P < 0.05

D I S C U S S I O N

The purpose of the current study was to evaluate the influence of altered attention focus by immersion in a virtual reality environment on step down performance in patients after ACLR. We employed a step down task to quantify differences in dynamics of the knee joint when different focus of attention was provided to the patients. A significant interaction was found between groups and environments for all outcome variables; GRF and peak internal extension knee moment. Interestingly, peak GRF values for the ACLR group when in virtual reality, approached those of healthy subjects. The influence of virtual reality was more pronounced in ACLR than in the CTRL group.The task had to be identical from a biomechanical perspective for both groups during both conditions. That was the primary reason why virtual reality was used to help control for attentional demands. It is difficult to meet these criteria for the practice of locomotor tasks in currently constrained indoor and outdoor settings. Virtual reality typically refers to the use of interactive simulations created with computer hardware and software to present users with opportunities to engage in environments that appear and feel similar to real world objects and events. Virtual reality enables researchers to analyze task performance in valid situations similar to real life, yet under experimentally controlled conditions.33

The influence of virtual reality was more pronounced in ACLR than in the CTRL group. We tested patients after ACLR in a not meaningful laboratory environment and a meaningful environment showing a real life scene to measure the changes in movement

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patterns. Although we have only studied the influence of the manipulated virtual environment on biomechanics of the knee, we suggest that this may have influenced the focus of attention. It needs to be recognized that attentional focus was not directly monitored to determine whether they were internally or externally focused. However we employed the virtual environment to invite subjects to a more external focus and from the results do we do assume that this may indeed be related to the focus of attention as this was the only manipulated variable. A recent study suggested that virtual reality promotes a dissociative attentional focus, acting as a “distractor” from the exercise performed.36

A continued internal focus may be detrimental to motor learning and even more detrimental to motor control restoration in patients following ACLR. When patients adopt an internal focus of attention, they are consciously focusing on the movement characteristics of their body.37 Research indicates that an external focus of attention enhances performance and motor learning.21 Instructions and feedback for motor skill learning during rehabilitation indicate that 95% of physical therapists provide feedback instructions with such an internal focus.38 A typical example is a clinician instructing a patient to straighten the knee more during the stance phase in gait. However, providing instructions that induce an external focus of attention have been shown to result in superior skill acquisition over using instructions that induce such internal foci of attention.39-42 For example, larger improvements in gait are achieved if gait training is coupled with virtual reality as compared to standard gait training.43,44

The benefits of an external focus have also been presented in patients suffering from an ankle sprain. The group practicing the acquisition of a postural skill task using an external focus significantly improved the ability to maintain balance, whereas those using an internal focus attention training program did not achieve significant improvement in balance measures.45

Several studies have shown that biomechanics (kinematics and kinetics) are not restored to normal levels after the surgical procedure.14,46,47 Recently, it was established that unilateral force development (vertical jump height) and absorption (normalized VGRF) persist in an athlete’s single-limb performance after ACLR that were not related to elapsed time after the surgery, although athletes after ACLR had returned to sports.20 Hence, after conclusion of the rehabilitation and clearance for return to sports, biomechanical deficits are still present indicating that current ACLR rehabilitation may not be optimally effective in addressing deficits related to the surgical intervention.48 Although there are good intuitive reasons to suggest a more novice-like mode of motor learning by inducing an internal focus in an attempt to target these asymmetries, this strategy may not be optimal.49 An internal focus results in an increase of co-contraction of agonists and antagonists, which in turn may cause “freezing” by limiting the degrees

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of freedom of movements, and in the recruitment of unnecessary motor units within muscles, which adds “noise” to the motor system.50

The clinical relevance of this study is that we were able to demonstrate that movement patterns can be modified in patients after ACLR using virtual reality. Perhaps virtual reality causes a decrease of the internal focus. In other words, less internal focus allows for more efficient movement performance.51 The current study may aid in our understanding how we can target leg asymmetries after ACLR. The incidence of a second injury to the ACLR knee or injury to the contralateral knee may exceed 20% in young athletes who returned to competitive activities.19 The most common biomechanical factor with increased risk of second injury is asymmetrical loading during sports related tasks.19,47

Cumulatively, the incorporation of external focus instructions into rehabilitation practice can potentially enhance the effectiveness and efficiency of rehabilitation. Current data shows that this can be realized by integrating easily available technology into rehabilitation programs to enhance motor learning capabilities with the ultimate goal to reduce risk of second injury risk. We acknowledge that virtual reality is not readily available to clinicians. In a recent RCT that compared a Nintendo Wii Fit (Nintendo, Kyoto, Japan) balance board program with conventional rehabilitation after ACLR, similar results were obtained in improving muscle strength, balance, and coordination and response time tasks.52 This type of technology can easily be integrated in daily practice. Several limitations of this study need to be acknowledged. No baseline data of ACLR subjects prior to surgery were available. A pre- and post-operative design may useful to directly assess the changes after ACLR. We have only studied the influence of the manipulated environment and only suggest that this may have influenced the focus of attention. It would have been beneficial to include questionnaires to gain a level of understanding regarding what participants focused on when performing the tasks.53

C O N C L U S I O N

The results of the current investigation indicate that patients after ACLR demonstrate altered movement patterns and loading of the involved knee at a time when they were cleared for return to sports. Embedding patients after ACLR in virtual reality changes their movement patterns approximating those of healthy subjects.

Conflict of interestThe authors have no conflicts of interest that are directly relevant to the content of this article.

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3. Gardinier ES, Manal K, Buchanan TS, Snyder-Mackler L. Gait and neuromuscular asymmetries after acute anterior cruciate ligament rupture. Med Sci Sports Exerc. 2012;44(8):1490-1496.

4. Castanharo R, da Luz BS, Bitar AC, D’Elia CO, Castropil W, Duarte M. Males still have limb asymmetries in multijoint movement tasks more than 2 years following anterior cruciate ligament reconstruction. J Orthop Sci. 2011;16(5):531-535.

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7. Paterno MV, Ford KR, Myer GD, Heyl R, Hewett TE. Limb Asymmetries in Landing and Jumping 2 Years Following Anterior Cruciate Ligament Reconstruction. Clin J Sport Med. 2007;17(4):258-262.

8. Patras K, Ziogas G, Ristanis S, Tsepis E, Stergiou N, Georgoulis AD. ACL reconstructed patients with a BPTB graft present an impaired vastus lateralis neuromuscular response during high intensity running. J Sci Med Sport. 2010;13(6):573-577.

9. Schmitt LC, Paterno MV, Hewett TE. The Impact of Quadriceps Femoris Strength Asymmetry on Functional Performance at Return to Sport Following Anterior Cruciate Ligament Reconstruction. J Orthop Sports Phys Ther. 2012;42(9):750-759.

10. Stergiou N, Ristanis S, Moraiti C, Georgoulis AD. Tibial Rotation in Anterior Cruciate Ligament (ACL)-Deficient and ACL-Reconstructed Knees : A Theoretical Proposition for the Development of Osteoarthritis. Sports Med. 2007;37(7):601-613.

11. Tashman S, Kolowich P, Collon D, Anderson K, Anderst W. Dynamic function of the ACL-reconstructed knee during running. Clin Orthop Relat Res. 2007;454:66-73.

12. Webster KE, Feller JA, Wittwer JE. Longitudinal changes in knee joint biomechanics during level walking following anterior cruciate ligament reconstruction surgery. Gait Posture. 2012;36(2):167-171.

13. Webster KE, Wittwer JE, O’Brien J, Feller JA. Gait patterns after anterior cruciate ligament reconstruction are related to graft type. Am J Sports Med. 2005;33(2):247-254.

14. Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal landing strategies after ACL reconstruction. Scand J Med Sci Sports. 2010;20(1):e12-19.

15. Hooper DM, Morrissey MC, Drechsler WI, Clark NC, Coutts FJ, McAuliffe TB. Gait analysis 6 and 12 months after anterior cruciate ligament reconstruction surgery. Clin Orthop Relat Res. 2002(403):168-178.

16. Hart JM, Ko JW, Konold T, Pietrosimone B. Sagittal plane knee joint moments following anterior cruciate ligament injury and reconstruction: a systematic review. Clin Biomech 2010;25(4):277-283.

17. Gokeler A, Benjaminse A, van Eck CF, Webster KE, Schot L, Otten E. Return of normal gait as an outcome measurement in ACL-reconstructed patients. A systematic review. Int J Sports Phys Ther. 2013;8(4):441-451.

18. Delahunt E, Sweeney L, Chawke M, et al. Lower limb kinematic alterations during drop vertical jumps in female athletes who have undergone anterior cruciate ligament reconstruction. J Orthop Res. 2012;30(1):72-78.

19. Paterno MV, Schmitt LC, Ford KR, et al. Biomechanical measures during landing and postural stability predict second anterior cruciate ligament injury after anterior cruciate ligament reconstruction and return to sport. Am J Sports Med. 2010;38(10):1968-1978.

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20. Myer GD, Martin L, Jr., Ford KR, et al. No association of time from surgery with functional deficits in athletes after anterior cruciate ligament reconstruction: evidence for objective return-to-sport criteria. Am J Sports Med. 2012;40(10):2256-2263.

21. Wulf G. Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc Psychol. 2012:1-28.

22. Schmidt RA WC. Motor learning and performance. Champaign, IL: Human Kinetics; 2005.

23. Shapiro L. Embodied Cognition. New York: Routledge Press; 2011.

24. Fitts PM, Possner MI. Human performance. Oxford, England: Brooks and Cole; 1967.

25. McNevin NH, Wulf G, Carlson C. Effects of attentional focus, self-control, and dyad training on motor learning: implications for physical rehabilitation. Phys Ther. 2000;80(4):373-385.

26. Benjaminse A, Lemmink KA, Diercks RL, Otten B. An investigation of motor learning during side-step cutting, design of a randomised controlled trial. BMC Musculoskelet Disord. 2010;11:235.

27. Chiviacowsky S, Wulf G, Wally R. An external focus of attention enhances balance learning in older adults. Gait Posture. 2010;32(4):572-575.

28. Masters RS, Lo CY, Maxwell JP, Patil NG. Implicit motor learning in surgery: implications for multi-tasking. Surgery. 2008;143(1):140-145.

29. Wulf G, McConnel N, Gartner M, Schwarz A. Enhancing the learning of sport skills through external-focus feedback. J Mot Behav. 2002;34(2):171-182.

30. Wulf G, Shea C, Park JH. Attention and motor performance: preferences for and advantages of an external focus. Res Q Exerc Sport. 2001;72(4):335-344.

31. Wulf G, McNevin N, Shea CH. The automaticity of complex motor skill learning as a function of attentional focus. Quart J Experim Psychol. Nov 2001;54(4):1143-1154.

32. Wulf G, Chiviacowsky S, Schiller E, Avila LT. Frequent external-focus feedback enhances motor learning. Front Psychol. 2010;1:190.

33. Adamovich SV, Fluet GG, Tunik E, Merians AS. Sensorimotor training in virtual reality: a review. Neuro Rehabil. 2009;25(1):29-44.

34. de Bruin ED, Schoene D, Pichierri G, Smith ST. Use of virtual reality technique for the training of motor control in the elderly. Some theoretical considerations. Z Gerontol Geriatr. 2010;43(4):229-234.

35. Myer GD, Schmitt LC, Brent JL, et al. Utilization of Modified NFL Combine Testing to Identify Functional Deficits in Athletes Following ACL Reconstruction. J Orthop Sports Phys Ther. 2011;41(6):377-387.

36. Mestre DR, Ewald M, Maiano C. Virtual reality and exercise: behavioral and psychological effects of visual feedback. Stud Health Technol Inform.2011;167:122-127.

37. Porter JM, Anton PM, Wikoff NM, Ostrowski JB. Instructing skilled athletes to focus their attention externally at greater distances enhances jumping performance. J Strength Cond Res. 2013;27(8):2073-2078.

38. Durham K, Van Vliet PM, Badger F, Sackley C. Use of information feedback and attentional focus of feedback in treating the person with a hemiplegic arm. Physiother Res Int. 2009;14(2):77-90.

39. Porter JM, Ostrowski EJ, Nolan RP, Wu WF. Standing long-jump performance is enhanced when using an external focus of attention. J Strength Cond Res. 2010;24(7):1746-1750.

40. Rotem-Lehrer N, Laufer Y. Effect of focus of attention on transfer of a postural control task following an ankle sprain. J Orthop Sports Phys Ther. 2007;37(9):564-569.

41. Wu WF, Porter JM, Brown LE. Effect of attentional focus strategies on peak force and performance in the standing long jump. J Strength Cond Res. 2012;26(5):1226-1231.

42. Wulf G, Dufek JS. Increased jump height with an external focus due to enhanced lower extremity joint kinetics. J Mot Behav. Oct 2009;41(5):401-409.

43. Lewek MD, Feasel J, Wentz E, Brooks FP, Jr., Whitton MC. Use of visual and proprioceptive feedback to improve gait speed and spatiotemporal symmetry following chronic stroke: a case series. Physical Ther. 2012;92(5):748-756.

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44. Mirelman A, Bonato P, Deutsch JE. Effects of training with a robot-virtual reality system compared with a robot alone on the gait of individuals after stroke. Stroke. 2009;40(1):169-174.

45. Laufer Y, Rotem-Lehrer N, Ronen Z, Khayutin G, Rozenberg I. Effect of attention focus on acquisition and retention of postural control following ankle sprain. Arch Phys Med Rehabil. 2007;88(1):105-108.

46. Ortiz A, Olson S, Trudelle-Jackson E, Rosario M, Venegas HL. Landing mechanics during side hopping and crossover hopping maneuvers in noninjured women and women with anterior cruciate ligament reconstruction. PM R. 2011;3(1):13-20.

47. Hewett TE, Di Stasi SL, Myer GD. Current concepts for injury prevention in athletes after anterior cruciate ligament reconstruction. Am J Sports Med. 2013;41(1):216-224.

48. Simoneau GG, Wilk KE. The challenge of return to sports for patients post-ACL reconstruction. J Orthop Sports Phys Ther. 2012;42(4):300-301.

49. Lohse KR, Sherwood DE, Healy AF. How changing the focus of attention affects performance, kinematics, and electromyography in dart throwing. Hum Mov Sci. 2010;29(4):542-555.

50. Lohse KR, Sherwood DE. Thinking about muscles: The neuromuscular effects of attentional focus on accuracy and fatigue. Acta Psychol. 2012;140(3):236-245.

51. Wulf G, Shea C, Lewthwaite R. Motor skill learning and performance: a review of influential factors. Med Educ. 2010;44(1):75-84.

52. Baltaci G, Harput G, Haksever B, Ulusoy B, Ozer H. Comparison between Nintendo Wii Fit and conventional rehabilitation on functional performance outcomes after hamstring anterior cruciate ligament reconstruction: prospective, randomized, controlled, double-blind clinical trial. Knee Surg Sports Traumatol Arthrosc. 2013;21(4):880-887.

53. Porter JM, Nolan RP, Ostrowski EJ, Wulf G. Directing attention externally enhances agility performance: a qualitative and quantitative analysis of the efficacy of using verbal instructions to focus attention. Front Psychol. 2010;1:216.

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S U M M A R Y

An injury of the anterior cruciate ligament (ACL) is one of the most common injuries in sports.1 In particular, young female athletes are at risk to sustain this devastating injury.2 It has become standard practice since the early nineties of the past millennium to perform an ACL reconstruction (ACLR) with the ultimate goal to allow athletes to resume their sports as prior to the injury.3 The two most common ACLR procedures are either the use of an autologous graft from the patellar tendon or the semintendinosis-gracilis tendon, of which the latter has become the most popular since the last decade.4 Despite an ACLR, there is no guarantee that the knee function will restore to the pre-injury level. It has been shown that for months and even years after ACLR deficits in 1) gait,5 2) running,6,7 3) balance,8,9 4) muscle strength,10,11 5) proprioception12,13 and 6) jumping and landing14-21 persist.The aim of this dissertation was to determine the effect of an ACL injury and subsequent ACLR on various motor skills and seek to find an explanation of the encountered observations.

In Chapter 2 the effect of quadriceps strength and anterior laxity on gait in patients six months after ACLR was analyzed. These two variables were postulated as causes for abnormal gait patterns in patients with ACL deficient (ACLD) knees.22 The contention is that patients with ACLD avoid activity of the quadriceps muscle as this may induce an anterior translation of the tibia, which may not be well controlled in case of an ACL injury. Hence, patients with ACLD limit the degrees of extension of the injured knee by keeping the knee in a stiff pattern of knee flexion. It was of interest to determine how restored laxity and quadriceps strength had an effect on gait patterns in patients after ACLR. Sagittal knee angles and knee moments during the stance phase were calculated. The most important findings were a reduced knee flexion and extension range of motion of the ACLR leg. In addition, the knee extension moment of the ACLR leg was significantly reduced. Most importantly, the results indicated that kinematic and kinetic gait parameters in ACLR knees were not related to quadriceps strength and laxity. If biomechanical deficits are present during a relative low load activity like gait, it is reasonable to assume that deficits are even more pronounced during high demanding activities like hopping. Hop tests are used as indicators of predetermined objective guidelines to determine a safe return to sports after ACLR.23,24 Typically, return to sports is often allowed as soon as six months after surgery.

The purpose of the study presented in Chapter 3 was to conduct a comprehensive assessment that included kinematic, kinetic and EMG-analysis during a single leg hop test for distance at six months after the surgical procedure. The results showed that

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in ACLR legs, significantly earlier onset times were found for all muscles, except the vastus medialis, compared with the uninvolved side. The involved legs had significantly reduced knee flexion during the take-off. In addition, increased plantarflexion angles of the ankle in the involved leg at initial contact during landing was observed. The knee extension moment was significantly lower in the involved leg. In the control group, significantly earlier onset times were found for the semitendinosus, vastus lateralis and medial gastrocnemius muscles of the non-dominant side compared with the dominant side. Differences in EMG onset times between the involved and the uninvolved leg in the patient group were significantly larger than differences between the dominant and the non-dominant side in healthy subjects, except for the semitendinosus, vastus lateralis and vastus medialis muscles. The studies carried out in Chapter 2 and 3 were merely descriptive in nature. A classical experimental scientific approach was employed in terms of performing an experiment and determine if there are statistical significant differences for the various dependent and independent variables. Subsequently, the data were then compared to data available in the literature to seek any similarities or discrepancies between our findings and those of others. Scientists then propose hypotheses as explanations of phenomena, and design experimental studies to test these hypotheses via predictions which can be derived from them. Research may become more valuable if a theory is available prior to conducting experiments. Theories that encompass wider domains of inquiry may bind independently derived hypotheses together in a coherent, supportive structure. Theories, in turn, may help form new hypotheses or place groups of hypotheses into context. Looking at science from that perspective, led to a different approach for the remaining chapters of this dissertation. It was decided that the focus of research should shift towards an understanding of the role of sensorimotor control after ACL injury. Sensorimotor control encompasses all the afferent, efferent, and central integration and processing components in human movement. The peripheral mechanoreceptors, and in particular the ‘’proprioceptors” have received the most attention from a clinical orthopaedic perspective. Proprioception is the afferent pathway relaying the acquisition of stimuli by articular, cutaneous and muscular and tendinous receptors to the central nervous system. As the ACL contains various receptors, it is plausible that a rupture of the ACL may result in altered motor control. Several studies have claimed that these proprioceptive deficits adversely affect activity level,25-27 balance,9,28 re-establishment of quadriceps strength29 and increase the risk of further injury.30

In Chapter 4, a systematic review was conducted to asses the role of proprioception on motor skills like balance, gait, hopping and strength in patients with ACLD or ACLR. In addition, we determined the association of proprioception and laxity of the knee as well

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as on patient reported outcome questionnaires. The correlation between proprioception and laxity, balance, hop tests and patient outcome was low. Only four studies reported a moderate correlation between proprioception, strength, balance, hop tests or gait. In conclusion, there is limited evidence that proprioceptive deficits as detected by commonly used tests adversely affect function in patients with ACLD and ACLR. Development of new tests to determine the relevant role of the sensorimotor system is needed. These tests should ideally be used as screening tests for primary and secondary prevention of ACL injury.The literature search clearly demonstrated that proprioceptive deficits certainly can not fully explain why altered movement occurs after ACLR. As stated before, proprioception entails only the afferent pathway of a sub-component of the sensorimotor system. However, effective motor control after an ACL injury and subsequent ACLR calls for efficient information processing between the entire body, brain and environment.

In the study as presented in Chapter 5, a new theoretical construct was proposed in that cognitive changes in motor control may have occurred after injury of the ACL and play a role in preventing return of normal movement patterns. The biomechanical studies that have been carried out in Chapter 2 and 3 offer descriptions of the changed movement patterns in patients after ACLR. In the acute phase after ACL-injury or subsequent ACLR, it may be useful that patients use a motor control program that is aimed at protection of the knee. Patients may take small steps, reduce the range of motion of the knee, limit the amount of weight on the involved leg and look very cautiously where they place the foot. The movements are further dictated by pain early after ACLR and may therefore serve a useful purpose. The contention is that patients after ACLR may utilize an increased cognitive focus on movement even months after surgery, which inhibits the learning process of regaining normal movements. It was hypothesized that patients after ACLR move in a more natural way - causing them to extend the boundaries of their constrained movement patterns - when they are immersed in a life-like virtual reality setting compared to a normal lab environment.It is difficult to meet these criteria for the practice of locomotor tasks in constrained indoor and outdoor settings. Virtual reality typically refers to the use of interactive simulations created with computer hardware and software to present users with opportunities to engage in environments that appear and feel similar to real world objects and events.31 The technology, with the capacity of simulating environments, offers a new and safe way to offer the varied environments and controlled constraints needed to maximize learning. In a virtual environment, the simulated objects and events are not only sensed, but the user can anticipate and react to them as though they are real. Virtual reality enables researchers to analyze task performance in valid

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situations similar to real life, yet under experimentally controlled conditions. That was the main reason why an experiment using virtual reality was chosen, in order to control for attentional demands, but performed within a functional environment or context. The results confirm indeed that movement patterns in ACLR patients while immersed in virtual reality, approached those of healthy subjects.

The final experiment of this dissertation sheds a new light on the often reported movement aberrations. Starting from a theoretical construct derived from the field of motor control science, a hypothesis was formulated that increased cognitive attentional control would play a role in movement patterns in patients with an ACLR. As the study in Chapter 5 showed, possible changes in attentional focus had a greater impact in patients after ACLR compared to healthy controls. This rises a question as to whether there is an effective coupling between the surgical procedure and the functional outcome in terms of return of normal movement patterns.

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R E F E R E N C E S1. Dick R, Hootman JM, Agel J, Vela L, Marshall SW, Messina R. Descriptive epidemiology of collegiate

women’s field hockey injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2002-2003. J Athl Train. 2007;42(2):211-220.

2. Renstrom P, Ljungqvist A, Arendt E, et al. Non-contact ACL injuries in female athletes: an International Olympic Committee current concepts statement. Br J Sports Med. 2008;42(6):394-412.

3. Shelbourne KD, Nitz P. Accelerated rehabilitation after anterior cruciate ligament reconstruction. Am J Sports Med. 1990;18(3):292-299.

4. Chechik O, Amar E, Khashan M, Lador R, Eyal G, Gold A. An international survey on anterior cruciate ligament reconstruction practices. Int Orthop. 2013;37(2):201-206.

5. Hart JM, Ko JW, Konold T, Pietrosimone B. Sagittal plane knee joint moments following anterior cruciate ligament injury and reconstruction: a systematic review. Clin Biomech. 2010;25(4):277-283.

6. Tashman S, Collon D, Anderson K, Kolowich P, Anderst W. Abnormal rotational knee motion during running after anterior cruciate ligament reconstruction. Am J Sports Med. 2004;32(4):975-983.

7. Tashman S, Kolowich P, Collon D, Anderson K, Anderst W. Dynamic function of the ACL-reconstructed knee during running. Clin Orthop Relat Res. 2007;454:66-73.

8. Henriksson M, Ledin T, Good L. Postural control after anterior cruciate ligament reconstruction and functional rehabilitation. Am J Sports Med. 2001;29(3):359-366.

9. Bonfim TR, Jansen Paccola CA, Barela JA. Proprioceptive and behavior impairments in individuals with anterior cruciate ligament reconstructed knees. Arch Phys Med Rehabil. 2003;84(8):1217-1223.

10. Keays SL, Bullock-Saxton JE, Newcombe P, Keays AC. The relationship between knee strength and functional stability before and after anterior cruciate ligament reconstruction. J Orthop Res. 2003;21(2):231-237.

11. Palmieri-Smith RM, Thomas AC, Wojtys EM. Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med. 2008;27(3):405-424.

12. Beynnon BD, Johnson RJ, Naud S, et al. Accelerated Versus Nonaccelerated Rehabilitation After Anterior Cruciate Ligament Reconstruction: A Prospective, Randomized, Double-Blind Investigation Evaluating Knee Joint Laxity Using Roentgen Stereophotogrammetric Analysis. Am J Sports Med. 2011;39(12):2536-2548.

13. Gokeler A, Benjaminse A, Hewett TE, et al. Proprioceptive deficits after ACL injury: are they clinically relevant? Br J Sports Med. 2012;46(3):180-192.

14. Castanharo R, da Luz BS, Bitar AC, D’Elia CO, Castropil W, Duarte M. Males still have limb asymmetries in multijoint movement tasks more than 2 years following anterior cruciate ligament reconstruction. J Orthop Sci. 2011;16(5):531-535.

15. Chmielewski TL. Asymmetrical lower extremity loading after ACL reconstruction: more than meets the eye. J Orthop Sports Phys Ther. 2011;41(6):374-376.

16. Delahunt E, Prendiville A, Sweeney L, et al. Hip and knee joint kinematics during a diagonal jump landing in anterior cruciate ligament reconstructed females. J Electromyogr Kinesiol. 2012;22(4):598-606.

17. Deneweth JM, Bey MJ, McLean SG, Lock TR, Kolowich PA, Tashman S. Tibiofemoral Joint Kinematics of the Anterior Cruciate Ligament-Reconstructed Knee During a Single-Legged Hop Landing. Am J Sports Med. 2010;38:(9)1820-1828.

18. Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal landing strategies after ACL reconstruction. Scand J Med Sci Sports. 2010;20(1):e12-19.

19. Myer GD, Martin L, Jr., Ford KR, et al. No Association of Time From Surgery With Functional Deficits in Athletes After Anterior Cruciate Ligament Reconstruction: Evidence for Objective Return-to-Sport Criteria. Am J Sports Med. 2012;40:(10):2256-2263

20. Ortiz A, Olson S, Libby CL, et al. Landing mechanics between noninjured women and women with anterior cruciate ligament reconstruction during 2 jump tasks. Am J Sports Med. 2008;36(1):149-157.

21. Paterno MV, Schmitt LC, Ford KR, Rauh MJ, Myer GD, Hewett TE. Effects of sex on compensatory landing strategies upon return to sport after anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2011;41(8):553-559.

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22. Berchuck M, Andriacchi TP, Bach BR, Reider B. Gait adaptations by patients who have a deficient anterior cruciate ligament. J Bone Joint Surg Am. 1990;72(6):871-877.

23. Bizzini M, Hancock D, Impellizzeri F. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: soccer. J Orthop Sports Phys Ther. 2012;42(4):304-312.

24. Waters E. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: basketball. J Orthop Sports Phys Ther. 2012;42(4):326-336.

25. Barrett DS. Proprioception and function after anterior cruciate reconstruction. J Bone Joint Surg Br. 1991;73(5):833-837.

26. Ochi M, Iwasa J, Uchio Y, Adachi N, Sumen Y. The regeneration of sensory neurones in the reconstruction of the anterior cruciate ligament. J Bone Joint Surg Br. 1999;81(5):902-906.

27. Roberts D, Friden T, Zatterstrom R, Lindstrand A, Moritz U. Proprioception in people with anterior cruciate ligament-deficient knees: comparison of symptomatic and asymptomatic patients. J Orthop Sports Phys Ther. 1999;29(10):587-594.

28. Jerosch J, Schaffer C, Prymka M. [Proprioceptive abilities of surgically and conservatively treated knee joints with injuries of the cruciate ligament]. Unfallchirurg. 1998;101(1):26-31.

29. Friden T, Roberts D, Ageberg E, Walden M, Zatterstrom R. Review of knee proprioception and the relation to extremity function after an anterior cruciate ligament rupture. J Orthop Sports Phys Ther. 2001;31(10):567-576.

30. Cooper RL, Taylor NF, Feller JA. A systematic review of the effect of proprioceptive and balance exercises on people with an injured or reconstructed anterior cruciate ligament. Res Sports Med. 2005;13(2):163-178.

31. Adamovich SV, Fluet GG, Tunik E, Merians AS. Sensorimotor training in virtual reality: a review. NeuroRehabilitation. 2009;25(1):29-44.

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S A M E N VAT T I N G

Een ruptuur van de voorste kruisband (VKB) is één van de meest voorkomende sportblessures.1 Vooral jonge vrouwelijke atleten lopen een verhoogd risico op deze ernstige blessure.2 Sinds de jaren negentig is het gebruikelijk een VKB-reconstructie te verrichten, met het ultieme doel sporters terug te laten keren naar het sportniveau van voor de blessure.3

De meest voorkomende VKB-reconstructietechnieken maken gebruik van een autoloog ent van de patellapees of semintendinosus-gracilispees, waarbij de laatstgenoemde het populairst is sinds het laatste decennium.4 Een VKB-reconstructie geeft echter niet de garantie dat de kniefunctie zal herstellen tot het niveau van voor de ruptuur. Het is aangetoond dat er maanden en zelfs jaren na VKB-reconstructie nog steeds deficiënties aanwezig kunnen zijn bij volgende: 1) lopen,5 2) hardlopen,6,7 3) balans,8,9 4) spierkracht,10,11 5) proprioceptie12,13 en 6) springen.14-21

De studies in dit proefschrift pogen te bepalen wat het effect is van een VKB-ruptuur, of specifieker: een VKB-reconstructie na een VKB-ruptuur, op diverse motorische vaardigheden en een verklaring voor de bevindingen te geven. Het doel van Hoofdstuk 2 is het effect te bepalen van de quadricepskracht en laxiteit op het gangbeeld in patiënten zes maanden na een VKB-reconstructie. Deze twee variabelen worden vaak als oorzaken gepostuleerd voor abnormale gangpatronen in patiënten met een VKB-ruptuur.22 De aanname is dat patiënten met een VKB-ruptuur activiteit van de m. quadriceps vermijden, aangezien deze een anterieure translatie van de tibia ten opzichte van het femur kan veroorzaken die onvoldoende kan worden gecontroleerd na een VKB-ruptuur. Om die reden beperken patiënten met een VKB-ruptuur de extensie van de knie door deze in een patroon van ‘stiff knee gait’ te bewegen met een beperkt flexie-extensietraject. In dit onderzoek is derhalve gekeken naar in hoeverre de herstelde laxiteit en kracht van de m. quadriceps een effect hebben op gangpatronen in patiënten na een VKB-reconstructie. De sagittale kniehoeken en kniemomenten zijn berekend tijdens de standfase van het lopen. De opvallendste bevindingen zijn een verminderde flexie en extensie bewegingssuitslag van het geopereerde been. Bovendien is gebleken dat het externe extensiemoment van de knie duidelijk verminderd is in het geopereerde been. Bovenal hebben de resultaten uitgewezen dat de gevonden kinematische en kinetische gangparameters na een VKB-reconstructie geen relatie hebben met de kracht van de M. quadriceps en laxiteit.

Als de biomechanische deficiënties tijdens een relatief lichte activiteit zoals lopen aanwezig zijn, is het redelijk om te veronderstellen dat de deficiënties meer uitgesproken zijn tijdens zwaardere activiteiten zoals springen.

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Gedurende de revalidatie worden vaak zogenaamde hoptesten (de single hop for distance, de 6-m timed hop test, de triple hop for distance en de crossover hop for distance) gebruikt. Deze hoptesten worden, aan de hand van objectieve richtlijnen, gebruikt als indicatoren om te bepalen wanneer een veilige terugkeer naar de sport na een VKB-reconstructie mogelijk is.23,24 Over het algemeen wordt deze terugkeer na zes maanden toegestaan. Het doel van de studie in Hoofdstuk 3 is een uitvoerige beoordeling van de single leg hop for distance zes maanden na de chirurgische procedure te verkrijgen die een integratie van kinematische, kinetische en EMG-analyses omvatte.

De resultaten hebben aangetoond dat VKB-reconstructie-benen een beduidend vroegere activatie hebben voor de volgende spieren: M. gluteus maximus, M. biceps femoris, M. semintendinosus, M. semimembranosus, M. vastus lateralis, M. rectus femoris, Mm. gastrocnemius caput mediale en laterale en M. soleus. De M. vastus medialis van het geopereerde been heeft een activatie vergelijkbaar met die van het niet-geopereerde been. In de controlegroep zijn de M. semitendinosus, M. vastus lateralis en M. gastrocnemius caput mediale beduidend vroeger geactiveerd aan de niet-dominante zijde dan aan de dominante zijde. De verschillen in EMG-begintijden tussen geopereerde en niet-geopereerde benen zijn beduidend groter dan de verschillen tussen de dominante en niet-dominante kant in de gezonde controlegroep, behalve voor de M. semitendinosus, M. vastus lateralis en M. vastus medialis. De geopereerde benen hebben aanzienlijk minder knieflexie bij de afzet van de sprong. Bij de landing is sprake gebleken van een toegenomen plantairflexie van de enkel. Het extensie moment van de knie is significant lager in het geopereerde been.

De studies die in Hoofdstuk 2 en 3 zijn uitgevoerd zijn beschrijvend van aard. Een klassieke wetenschappelijke benadering is aangewend voor het uitvoeren van een experiment waarbij bepaald is of er sprake was van statistisch significante verschillen voor de diverse afhankelijke en onafhankelijke variabelen. Later zijn deze gegevens vergeleken met beschikbare gegevens in de literatuur. Wetenschappers stellen hypothesen op om fenomenen te verklaren en ontwerpen experimentele studies om deze hypothesen te testen. Wetenschappelijk onderzoek kan waardevoller worden als een theorie voorafgaand aan het uitvoeren van experimenten beschikbaar is. De theorieën die bredere domeinen van onderzoek omvatten kunnen vele onafhankelijk afgeleide hypothesen in een coherente, steunende structuur samenbinden. Die theorieën kunnen helpen nieuwe hypothesen te vormen of groepen hypothesen in context te plaatsen. Dit perspectief op wetenschap heeft tot een andere benadering voor de resterende hoofdstukken van dit proefschrift geleid. We hebben besloten dat

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de nadruk van het verdere onderzoek naar de rol van sensomotorische controle na een VKB-ruptuur zou moeten verschuiven. Door een perifere observatie van het kniegewricht zijn wij geïnteresseerd geraakt in de rol van sensomotoriek. Onder sensomotoriek wordt de integratie en verwerking van alle afferente, efferente en centrale componenten die betrokken zijn bij het handhaven van de functionele stabiliteit van het gewricht verstaan.Proprioceptie is de afferente informatie afkomstig van stimuli van gewrichts-, huid-, spier- en peesrecepetoren die wordt voortgeleid aan het centrale zenuwstelsel. Aangezien de VKB diverse receptoren bevat, is het aannemelijk dat een VKB-ruptuur in een veranderde motorische controle kan resulteren. Verscheidene onderzoekers beweren dat deze proprioceptieve deficiënties kunnen leiden tot negatieve effecten op het activiteitenniveau,25-27 de balans9,28 en de M. quadricepsspierkracht29. Daarnaast kan sprake zijn van een verhoogd risico op verdere blessures.30 In Hoofdstuk 4 worden de resultaten beschreven van een systematic review naar de relatie tussen proprioceptie en balans, lopen, springen (hoptesten) en spierkracht in patiënten met een VKB-ruptuur of VKB-reconstructie. Bovendien hebben wij de relatie tussen proprioceptie en patiëntvragenlijsten bekeken. In het algemeen is de relatie tussen proprioceptie en laxiteit, balans, hoptesten en patiëntvragenlijsten laag gebleken. Slechts vier studies melden een matige relatie tussen proprioceptie, spierkracht, balans, hoptesten en het lopen. Samenvattend: er is slechts beperkt bewijs dat de proprioceptieve deficiënties de kniefunctie ongunstig beïnvloeden in patiënten met een VKB-ruptuur of VKB-reconstructie. Het is nodig nieuwe tests te ontwikkelen om beter inzicht te krijgen in de werking van het sensorimotorisch systeem na een VKB-ruptuur. Deze tests zouden idealiter als screening kunnen worden gebruikt om primaire en secundaire preventie van VKB-rupturen te optimaliseren.

In Hoofdstuk 2 en 3 hebben we beschrijvende studies gepresenteerd met betrekking tot de veranderde bewegingspatronen in patiënten met een VKB-reconstructie. In ons onderzoek, dat is ontsprongen in perifere observaties over bijvoorbeeld spierkracht en laxitieit van de knie, hebben wij vervolgens de invloed van proprioceptie op de waargenomen bewegingspatronen bekeken. Ons literatuuronderzoek heeft duidelijk aangetoond dat de proprioceptieve deficieten deze veranderingen in het bewegen niet volledig kunnen verklaren. Zoals eerder vermeld, behelst proprioceptie slechts de afferente weg van een subcomponent van het sensorimotorisch systeem. Een efficiënte motorische controle na een VKB-ruptuur, eventueel gevolgd door een VKB-reconstructie, vraagt om een efficiënte informatieoverdracht tussen het lichaam, het brein en de omgeving. In de studie die in Hoofdstuk 5 wordt gepresenteerd, stellen wij een nieuwe theoretische verklaring voor waarin cognitieve veranderingen in de motorische controle optreden na een VKB-ruptuur en deze de terugkeer naar

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normale bewegingspatronen verhinderen. In de acute fase na een VKB-ruptuur of VKB-reconstructie kan het nuttig zijn dat patiënten een motorisch programma volgen dat volledig is gericht op bescherming van de knie. De patiënten kunnen maatregelen treffen om de bewegingsuitslag van de knie te verminderen, de hoeveelheid gewicht op het geopereerde been te beperken en aandachtig te kijken naar waar zij de voet plaatsen tijdens het lopen. De bewegingen worden verder bepaald door pijn in de vroege fase na een VKB-reconstructie en kunnen daarom een nuttig doel dienen. Ons standpunt is dat bij de patiënten na een VKB-reconstructie tijdens het bewegen sprake is van een verhoogde cognitieve aandacht die het leerproces om normale bewegingen te herwinnen remt. Wij hebben de hypothese opgesteld dat de patiënten na een VKB-reconstructie op een natuurlijkere manier bewegen in een virtual reality-omgeving dan in een klassiek laboratoriummilieu. Bij virtual reality wordt met behulp van een computer een omgeving gesimuleerd die diverse zintuigen prikkelt. Deze technologie biedt een nieuwe en veilige manier om gevarieerde omgevingen aan te bieden waarin motorisch leren onderzocht kan worden.31 In een virtuele omgeving kunnen de gebruikers niet alleen de gesimuleerde voorwerpen en gebeurtenissen ontdekken, maar er ook op anticiperen en reageren alsof zij echt zijn. De virtuele werkelijkheid stelt onderzoekers in staat om taken te analyseren in relevante omgevingen die overeenkomen met die in het dagelijks leven, maar in een gecontroleerde experimentele setting. Dat is de belangrijkste reden waarom wij voor virtual reality hebben gekozen. De setting heeft het mogelijk gemaakt om voor de variabele aandacht te controleren. Het is belangrijk dat de bewegingen binnen een functionele omgeving of een context worden uitgevoerd. Onze resultaten bevestigen dat de bewegingspatronen in patiënten na een VKB-reconstructie bij een afstaptaak in de virtual reality die van gezonde proefpersonen benaderden. Het laatste experiment van deze thesis werpt een nieuw licht op de vaak beschreven afwijkende bewegingspatronen. Vanuit een theoretisch concept dat is afgeleid uit kennis op het gebied van de motorische controle, is de hypothese geformuleerd dat cognitieve aandacht een rol kan spelen in bewegingspatronen in patiënten met een VKB-reconstructie. Onze studie heeft aangetoond dat veranderingen in aandacht een grotere invloed hebben in patiënten na een VKB-reconstructie dan in gezonde controles. Dit roept de vraag op of er een efficiënte koppeling bestaat tussen de chirurgische procedure en het functionele resultaat betreffende de terugkeer naar normale bewegingspatronen.

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R E F E R E N T I E S1. Dick R, Hootman JM, Agel J, Vela L, Marshall SW, Messina R. Descriptive epidemiology of collegiate

women’s field hockey injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2002-2003. J Athl Train. 2007;42(2):211-220.

2. Renstrom P, Ljungqvist A, Arendt E, et al. Non-contact ACL injuries in female athletes: an International Olympic Committee current concepts statement. Br J Sports Med. 2008;42(6):394-412.

3. Shelbourne KD, Nitz P. Accelerated rehabilitation after anterior cruciate ligament reconstruction. Am J Sports Med. 1990;18(3):292-299.

4. Chechik O, Amar E, Khashan M, Lador R, Eyal G, Gold A. An international survey on anterior cruciate ligament reconstruction practices. Int Orthop. 2013;37(2):201-206.

5. Hart JM, Ko JW, Konold T, Pietrosimone B. Sagittal plane knee joint moments following anterior cruciate ligament injury and reconstruction: a systematic review. Clin Biomech. 2010;25(4):277-283.

6. Tashman S, Collon D, Anderson K, Kolowich P, Anderst W. Abnormal rotational knee motion during running after anterior cruciate ligament reconstruction. Am J Sports Med. 2004;32(4):975-983.

7. Tashman S, Kolowich P, Collon D, Anderson K, Anderst W. Dynamic function of the ACL-reconstructed knee during running. Clin Orthop Relat Res. 2007;454:66-73.

8. Henriksson M, Ledin T, Good L. Postural control after anterior cruciate ligament reconstruction and functional rehabilitation. Am J Sports Med. 2001;29(3):359-366.

9. Bonfim TR, Jansen Paccola CA, Barela JA. Proprioceptive and behavior impairments in individuals with anterior cruciate ligament reconstructed knees. Arch Phys Med Rehabil. 2003;84(8):1217-1223.

10. Keays SL, Bullock-Saxton JE, Newcombe P, Keays AC. The relationship between knee strength and functional stability before and after anterior cruciate ligament reconstruction. J Orthop Res. 2003;21(2):231-237.

11. Palmieri-Smith RM, Thomas AC, Wojtys EM. Maximizing quadriceps strength after ACL reconstruction. Clin Sports Med. 2008;27(3):405-424.

12. Beynnon BD, Johnson RJ, Naud S, et al. Accelerated Versus Nonaccelerated Rehabilitation After Anterior Cruciate Ligament Reconstruction: A Prospective, Randomized, Double-Blind Investigation Evaluating Knee Joint Laxity Using Roentgen Stereophotogrammetric Analysis. Am J Sports Med. 2011;39(12):2536-2548.

13. Gokeler A, Benjaminse A, Hewett TE, et al. Proprioceptive deficits after ACL injury: are they clinically relevant? Br J Sports Med. 2012;46(3):180-192.

14. Castanharo R, da Luz BS, Bitar AC, D’Elia CO, Castropil W, Duarte M. Males still have limb asymmetries in multijoint movement tasks more than 2 years following anterior cruciate ligament reconstruction. J Orthop Sci. 2011;16(5):531-535.

15. Chmielewski TL. Asymmetrical lower extremity loading after ACL reconstruction: more than meets the eye. J Orthop Sports Phys Ther. 2011;41(6):374-376.

16. Delahunt E, Prendiville A, Sweeney L, et al. Hip and knee joint kinematics during a diagonal jump landing in anterior cruciate ligament reconstructed females. J Electromyogr Kinesiol. 2012;22(4):598-606.

17. Deneweth JM, Bey MJ, McLean SG, Lock TR, Kolowich PA, Tashman S. Tibiofemoral Joint Kinematics of the Anterior Cruciate Ligament-Reconstructed Knee During a Single-Legged Hop Landing. Am J Sports Med. 2010;38:(9)1820-1828.

18. Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal landing strategies after ACL reconstruction. Scand J Med Sci Sports. 2010;20(1):e12-19.

19. Myer GD, Martin L, Jr., Ford KR, et al. No Association of Time From Surgery With Functional Deficits in Athletes After Anterior Cruciate Ligament Reconstruction: Evidence for Objective Return-to-Sport Criteria. Am J Sports Med. 2012;40:(10):2256-2263

20. Ortiz A, Olson S, Libby CL, et al. Landing mechanics between noninjured women and women with anterior cruciate ligament reconstruction during 2 jump tasks. Am J Sports Med. 2008;36(1):149-157.

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21. Paterno MV, Schmitt LC, Ford KR, Rauh MJ, Myer GD, Hewett TE. Effects of sex on compensatory landing strategies upon return to sport after anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2011;41(8):553-559.

22. Berchuck M, Andriacchi TP, Bach BR, Reider B. Gait adaptations by patients who have a deficient anterior cruciate ligament. J Bone Joint Surg Am. 1990;72(6):871-877.

23. Bizzini M, Hancock D, Impellizzeri F. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: soccer. J Orthop Sports Phys Ther. 2012;42(4):304-312.

24. Waters E. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: basketball. J Orthop Sports Phys Ther. 2012;42(4):326-336.

25. Barrett DS. Proprioception and function after anterior cruciate reconstruction. J Bone Joint Surg Br. 1991;73(5):833-837.

26. Ochi M, Iwasa J, Uchio Y, Adachi N, Sumen Y. The regeneration of sensory neurones in the reconstruction of the anterior cruciate ligament. J Bone Joint Surg Br. 1999;81(5):902-906.

27. Roberts D, Friden T, Zatterstrom R, Lindstrand A, Moritz U. Proprioception in people with anterior cruciate ligament-deficient knees: comparison of symptomatic and asymptomatic patients. J Orthop Sports Phys Ther. 1999;29(10):587-594.

28. Jerosch J, Schaffer C, Prymka M. [Proprioceptive abilities of surgically and conservatively treated knee joints with injuries of the cruciate ligament]. Unfallchirurg. 1998;101(1):26-31.

29. Friden T, Roberts D, Ageberg E, Walden M, Zatterstrom R. Review of knee proprioception and the relation to extremity function after an anterior cruciate ligament rupture. J Orthop Sports Phys Ther. 2001;31(10):567-576.

30. Cooper RL, Taylor NF, Feller JA. A systematic review of the effect of proprioceptive and balance exercises on people with an injured or reconstructed anterior cruciate ligament. Res Sports Med. 2005;13(2):163-178.

31. Adamovich SV, Fluet GG, Tunik E, Merians AS. Sensorimotor training in virtual reality: a review. NeuroRehabilitation. 2009;25(1):29-44.

Chapter 7General Discussion

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The journey of this dissertation started with an investigation to determine differences during gait between cohorts of patients with ACLD and ACLR.1 Interestingly, a majority of the patients with ACLD displayed more normal gait patterns in terms of side to side symmetry when compared to an ACLR group. Our findings showed that the return of normal gait may even take more than one year in patients following ACL injury and specifically ACLR. Interestingly, six months after ACLR is usually the time period when patients are allowed to return to sports.2-4

This preliminary study instigated a 10 year journey to finish this dissertation that is aimed to determine the most effective rehabilitation strategies in patients following ACLR. As patients after ACLR in whom a patellar tendon autograft was used, showed significant abnormalities in this study, an interest was triggered as to what could explain the nature of aberrant movement patterns during gait after ACLR. Gait analysis as conducted six months after ACLR, demonstrated that a reduced knee range of motion extension and reduced knee extension moment was used by these patients. Berchuk and co-workers introduced the term quadriceps avoidance.5 They postulated that patients with ACLD altered their gait by avoiding the anterior displacement of the tibia by reducing the quadriceps activity that is normally present when the knee is near full extension.5 It could be argued that patients after ACLR also demonstrate the purported quadriceps avoidance gait to protect the knee from excessive anterior translation of the tibia by reducing the amount of extension during stance.

The results in Chapter 2 however, demonstrate that a quadriceps avoidance gait did not occur in our patients6 after ACLR which is in agreement with others.7 Confirming our earlier work, patients after ACLR displayed reduced knee extension range of motion as well as a reduced internal extension moment of the knee.1 Moreover, neither anterior laxity nor quadriceps strength was related to the abnormal gait patterns. It is important to note that all patients had full passive extension of the knee. However, as a group they did not utilize these degrees of freedom the joint allowed them to. If the ACLR leg is not symmetrically loaded compared to the uninvolved side during gait, one would expect the same strategy to be present during high loading activities. Jumping is such an activity, and as such various hop tests are advocated in the literature to determine readiness to return to sports after ACLR. These tests have traditionally been conducted in a time dependent scheme after ACLR, usually at six months after surgery, however some use them even as early as four months.2,8

In Chapter 3 it was shown that six months after ACLR, patients jumped with adapted neuromuscular and biomechanical strategies during a single leg hop task. This could potentially lead to increased risk for second injury. It has recently been shown that

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patients who have had an ACLR, have increased risk to sustain the same injury, mainly on the contralateral side, when compared to non injured subjects.9 The incidence of second injury has been reported to be 15 times greater than that of control subjects.9 In other words, an initial ACL injury itself increases risk for second injury. Split by gender, female athletes following ACLR demonstrated 16 times greater rate of recurrent injury than female control subjects.9 In addition, female athletes were four times more likely to suffer a second ACL injury and six times more likely than male athletes to suffer a contralateral injury.10 Biomechanical risk factors associated with the second injury are balance deficits, increased valgus movement of the knee, greater asymmetry in internal knee extension moment and a deficit in hip internal rotation moment at the uninvolved side at initial contact.9 Right now, the general prevailing thought is that increased risk is potentially due to altered movement patterns and poor neuromuscular control.

However the causes of these increased risk factors due to altered movement patterns are not fully understood or reported in the literature. In our journey, moving from the peripheral explanations like quadriceps strength and laxity of the knee, we chose to evaluate the role of proprioception as part of the explanation on the observed movement patterns in Chapter 4. In an extensive review of the literature, there were no strong relationships found between proprioception and motor skills like balance and hopping. As such, the role of prioception seems to be overrated. Valeriani et al. examined the somatosensory-evoked potentials in ACL injured patients before and after surgery.11 They detected altered somatosensory-evoked potentials in a number of patients and proposed that ACL injury leads to changed ascending afferent pathways that may cause reorganization of the central nervous system (CNS). Recently, ACLD was shown to alter motor activity of the CNS.12 Such evidence could help to explain clinical symptoms that accompanied the above mentioned altered movement patterns. Another possibility is that patients have ineffective motor learning strategies. The patients after ACLR demonstrated persistent asymmetry during the gait and jump tasks respectively. It has recently been reported that deficits in force generation and absorption during a vertical jump task are not related to time after surgery.13 If deficits are not effectively addressed in the early stages after ACLR, they may carry over to other, more difficult motor skills later on. The issues addressed above, indicate that current rehabilitation programs have not been successful in training patients to load both legs in a symmetrical fashion.14 If the causes of these abnormal movement patterns are known, rehabilitation programs can be developed and implemented to determine if and how these alterations can be normalized or optimized.

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In our effort to understand the described differences in movement patterns in Chapter 2 and 3, we conducted the virtual reality study (Chapter 5). We wanted to investigate whether patients following ACLR would move in a more natural way when immersed in a life-like virtual reality setting. The changes in attentional focus, from internal to external, had a greater impact in ACLR patients compared to healthy controls. This raises the question as to whether there is an effective coupling between the surgical procedure and the functional outcome in terms of improved or return of normal movement patterns. Motor learning is the process of an individual’s ability to acquire motor skills with a relatively permanent change.15 It appears that patients after ACLR as studied in Chapter 5 are not fully capable of using the potential of plasticity of motor learning. Effective motor control calls for an efficient information processing between the body, brain and environment (embodied cognition).16 The motor system has the ability to adapt to environmental constraints and injury to itself. In case of a normal scenario, one would expect that patients after ACLR would fully recover in terms of restoration of normal movement patterns as prior to the injury. Evidence however is emerging that movement patterns may not fully restore after ACLR.9,13,17-28

The reasons as to why patients after ACLR may not accomplish normal movement patterns are probably multi-factorial in nature. These factors will be briefly outlined in the following section and a paradigm change in presented. First, changes in the sensorimotor system need to be considered. It has been shown that an ACL injury causes direct changes in the CNS. Recent studies have shown that altered activity of the motor cortex is present both in ACLD patients as well after ACLR.11,12,29,30 For example, patients with ACLD who were able to participate in sports despite a ruptured ACL had changes in central sensory representation when compared to patients with ACLD who experience instability of the knee.31 Based on the aforementioned, a ruptured ACL should be regarded also as a neurophysiological lesion instead of only a simple musculoskeletal lesion.Secondly, the fear-avoidance model (FAM) may be applied to patients after ACLR. The FAM is a biopsycho-social model proposed to explain the development of chronic disability after musculoskeletal injury.32 The FAM proposes that when pain is perceived as a threat following musculoskeletal injury, various psychosocial constructs, such as increased pain catastrophizing and fear of movement or reinjury, are altered, leading to disuse, depression, disability, and higher pain levels. Recently, improvements in self-efficacy for rehabilitation tasks and fear of movement or reinjury were shown to be predictors of improvements in knee pain and function.33

Third, the paradigm change that is presented is based on the results of Chapter 5

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shedding a different light on the results of Chapters 2 and 3. The contention as outlined in this dissertation, is that patients after ACLR may utilize an increased attentional, cognitive focus on movement which inhibits the learning process of regaining normal movements.

During the immediate period after ACLR, the execution of movement requires attention as directed by physical therapists and physicians, so that there exists also a dependency on cognitive control. In earlier research it was postulated that throughout the learning stages, dependency on cognitive and visual control of movement diminish in the final stages of learning in that execution of motor skills become automatic again.34 Patients after ACLR may fail to advance to the more autonomous phases of motor control, and a result demonstrate altered movement patterns that are governed by too much cognitive control. The postulated causes of altered movement pattern after ACLR need to be more explored in future.

I M P L I C AT I O N S F O R R E H A B I L I TAT I O N

As a continuum of these findings, we reviewed literature related to motor learning research. It is common in rehabilitation settings to provide instructions and feedback to facilitate motor skill learning during rehabilitation. Typically, the feedback is directed at the various components of the movement. The treating clinician may tell a patient who has an altered gait pattern after ACLR, to extend the knee more during the stance phase. In motor learning, this type of attentional focus is termed “internal focus” as it induces the performer’s attention directed towards the actual movements produced.35 Conversely, an external focus of attention is induced when a performer’s attention is directed towards an outcome or the effects of the movement being produced (e.g., “imagine to kick a ball”, to facilitate extension of the knee). Prior reports indicate that 95% of physical therapists provide feedback instructions with such an internal focus.36 Research is evolving that indicates this type of instructing with this type attentional focus may not be as effective as previously thought.37 Traditionally, instructions during landing from jumping are directed towards the execution of the movements itself. Often used instructions are “keep the knee over the toe”; “land with a slightly flexed knee”; “raise the knee to the level of the hip” or “land with your feet shoulder-width apart”.2,38 Although, there are intuitive reasons that clinicians give internally focused instructions, this approach may even foster more difficulty in patients following ACLR to re-learn skills. Such an internal focus results in an increase of co-contraction which in turn may cause “freezing” by limiting the degrees of freedom of movements.37

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More recently, Wulf and Lewthwaite expanded this explanation by suggesting that the mere mention of the participant’s body parts provokes a focus on the patient him-/herself.39 The self-construct has increasingly been recognized as an important factor within social environments, influencing individuals’ thoughts, actions, and behavior, often implicitly.40 The fact that motor performance often takes place in the presence of others and can be evaluated by them, may in and of itself lead to a state of self-consciousness and subsequent self-evaluation. This, in turn, can lead to “micro-choking” episodes and a switching of attention to self-regulatory activity.39 Efforts to manage self-related thoughts and emotions may be so demanding that available attentional capacity is exceeded and performance suffers. It is also conceivable that these processes promote a conscious control of both movement and self-regulatory activities.41 Considering that feedback, by its nature, implies an evaluation of an individual’s performance, it may not be surprising that frequent feedback can have detrimental effects compared to less frequent feedback.42 These effects are most likely exacerbated when individuals are provided with specific body-related or internal-focus feedback. In contrast, the “self-invoking trigger” does not come into play when the feedback promotes an external focus.35,43,44 In fact, frequent external-focus feedback seems to serve as a potent reminder to maintain beneficial effects on performance and learning.45

Of interest, in most rehabilitation situations, clinicians determine the details of the training session. They decide, for example, on the order of practice tasks, practice duration, and when or if feedback will be provided or demonstrations given. Thus, whereas clinicians generally control most aspects of practice, patients assume a relatively passive role. Yet there is converging evidence that the effectiveness of skill learning can be enhanced if the patient is given some control over the practice conditions. That is, a certain degree of self-control can result in more effective learning than completely prescribed training protocols.46,47 Finally, motor learning seems to be enhanced by positive relative to negative normative feedback.48,49 Negative normative feedback on the other hand may hamper motor learning. This finding of impaired learning with indications of poor performance is in line with the findings of several recent studies which demonstrated that feedback provided after “poor” trials is not as effective for learning as feedback provided after “good” trials50 and that negative normative feedback degrades learning relative to positive social-comparative feedback.39,51 Empirically, clinicians often provide feedback in terms of correcting the patient’s faulty performance of a given task.2 However, beliefs about personal capability have been shown to affect performance. The results of aforementioned studies also highlight the role of motivational influences on motor learning.52 In summary, it is worthwhile to give patients positive remarks to enhance learning.

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F U T U R E D I R E C T I O N S

Although this dissertation can only answer a small percentage of all variables involved in aberrant movement patterns, several interesting findings were revealed that may change rehabilitation programs following ACLR. Most athletes who wish to continue sports after an injury to the ACL are advised to undergo surgical reconstruction of the ligament.3 Nevertheless, reconstruction of the ACL does not equate to normal function of the knee or reduced risk of subsequent injuries. Injury rates for a second injury exceed 20% for young highly active athletes returning to sports within the first year after surgery.9 In Sweden, 22% of the 15- to 18-year-old female soccer players reported a revision or contralateral ACLR during a 5-year period.53 Recently, it was shown that return to a high activity level after a unilateral ACLR was the most important risk factor of sustaining a contralateral ACL injury.54

There is a plethora of data available that indicates that biomechanics are altered after ACLR that persist for several years and likely increase risk for injury to the contralateral side.9 Given this outcome, it appears that current rehabilitation programs may not provide effective stimuli to patients after ACLR to improve their altered movement patterns and prevent secondary injury.14 Novel training methods may target asymmetrical movement patterns in patients following ACLR during activities that may pose athletes at risk for re-injury. Insight gained from recent motor learning research and current dissertation may improve the effectiveness of secondary prevention of ACL injury and outcome in terms of returning to pre-injury athletic levels. The effect of factors like external focus, self-controlled learning and positive feedback should be investigated in rehabilitation after ACLR. Ideally, future rehabilitation employing principles from motor learning could be implemented to successfully target increased risk of second injury and reduce or delay the onset of osteoarthritis.

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R E F E R E N C E S1. Schmalz T, Blumentritt S, Wagner R, Gokeler A. Gait analysis of patients within one year after anterior

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2. Wilk KE, Macrina LC, Cain EL, Dugas JR, Andrews JR. Recent advances in the rehabilitation of anterior cruciate ligament injuries. J Orthop Sports Phys Ther. 2012;42(3):153-171.

3. Marx RG, Jones EC, Angel M, Wickiewicz TL, Warren RF. Beliefs and attitudes of members of the American Academy of Orthopaedic Surgeons regarding the treatment of anterior cruciate ligament injury. Arthroscopy. 2003;19(7):762-770.

4. Adams D, Logerstedt DS, Hunter-Giordano A, Axe MJ, Snyder-Mackler L. Current concepts for anterior cruciate ligament reconstruction: a criterion-based rehabilitation progression. J Orthop Sports Phys Ther. 2012;42(7):601-614.

5. Berchuck M, Andriacchi TP, Bach BR, Reider B. Gait adaptations by patients who have a deficient anterior cruciate ligament. J Bone Joint Surg Am. 1990;72(6):871-877.

6. Gokeler A, Schmalz T, Knopf E, Freiwald J, Blumentritt S. The relationship between isokinetic quadriceps strength and laxity on gait analysis parameters in anterior cruciate ligament reconstructed knees. Knee Surg Sports Traumatol Arthrosc. 2003;11(6):372-378.

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9. Paterno MV, Schmitt LC, Ford KR, et al. Biomechanical measures during landing and postural stability predict second anterior cruciate ligament injury after anterior cruciate ligament reconstruction and return to sport. Am J Sports Med. 2010;38(10):1968-1978.

10. Paterno MV, Rauh MJ, Schmitt LC, Ford KR, Hewett TE. Incidence of Contralateral and Ipsilateral Anterior Cruciate Ligament (ACL) Injury After Primary ACL Reconstruction and Return to Sport. Clin J Sport Med. 2012;22(2):116-121.

11. Valeriani M, Restuccia D, Di Lazzaro V, Franceschi F, Fabbriciani C, Tonali P. Clinical and neurophysiological abnormalities before and after reconstruction of the anterior cruciate ligament of the knee. Acta Neurol Scand. 1999;99(5):303-307.

12. Kapreli E, Athanasopoulos S, Gliatis J, et al. Anterior cruciate ligament deficiency causes brain plasticity: a functional MRI study. Am J Sports Med. 2009;37(12):2419-2426.

13. Myer GD, Martin L, Jr., Ford KR, et al. No association of time from surgery with functional deficits in athletes after anterior cruciate ligament reconstruction: evidence for objective return-to-sport criteria. Am J Sports Med. 2012;40(10):2256-2263.

14. Simoneau GG, Wilk KE. The challenge of return to sports for patients post-ACL reconstruction. J Orthop Sports Phys Ther. 2012;42(4):300-301.

15. Schmidt RA WC. Motor learning and performance. Champaign, IL: Human Kinetics; 2005.

16. Shapiro L. Embodied Cognition. New York: Routledge Press; 2011.

17. Ageberg E, Thomee R, Neeter C, Silbernagel KG, Roos EM. Muscle strength and functional performance in patients with anterior cruciate ligament injury treated with training and surgical reconstruction or training only: a two to five-year followup. Arthritis Rheum. 2008;59(12):1773-1779.

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18. Butler RJ, Minick KI, Ferber R, Underwood F. Gait mechanics after ACL reconstruction: implications for the early onset of knee osteoarthritis. Br J Sports Med. 2009;43(5):366-370.

19. Chmielewski TL. Asymmetrical lower extremity loading after ACL reconstruction: more than meets the eye. J Orthop Sports Phys Ther. 2011;41(6):374-376.

20. Decker MJ, Torry MR, Noonan TJ, Riviere A, Sterett WI. Landing adaptations after ACL reconstruction. Med.Sci.Sports Exerc. 2002;34(9):1408-1413.

21. Delahunt E, Prendiville A, Sweeney L, et al. Hip and knee joint kinematics during a diagonal jump landing in anterior cruciate ligament reconstructed females. J Electromyogr Kinesiol. 2012;22(4):598-606.

22. Georgoulis AD, Ristanis S, Moraiti C, Mitsou A, Bernard M, Stergiou N. Three-dimensional kinematics of the tibiofemoral joint in ACL-deficient and reconstructed patients shows increased tibial rotation. Operat Techn Orthop. 2005;15(1):49-56.

23. Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal landing strategies after ACL reconstruction. Scand J Med Sci Sports. 2010;20(1):e12-19.

24. Knoll Z, Kocsis L, Kiss RM. Gait patterns before and after anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2004;12(1):7-14.

25. Ortiz A, Olson S, Libby CL, et al. Landing mechanics between noninjured women and women with anterior cruciate ligament reconstruction during 2 jump tasks. Am J Sports Med. 2008;36(1):149-157.

26. Paterno MV, Ford KR, Myer GD, Heyl R, Hewett TE. Limb Asymmetries in Landing and Jumping 2 Years Following Anterior Cruciate Ligament Reconstruction. Clin J Sport Med. 2007;17(4):258-262.

27. Castanharo R, da Luz BS, Bitar AC, D’Elia CO, Castropil W, Duarte M. Males still have limb asymmetries in multijoint movement tasks more than 2 years following anterior cruciate ligament reconstruction. J Orthop Sci. 2011;16(5):531-535.

28. Logerstedt D, Lynch A, Axe MJ, Snyder-Mackler L. Symmetry restoration and functional recovery before and after anterior cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2013;21(4):859-868.

29. Baumeister J, Reinecke K, Schubert M, Weiss M. Altered electrocortical brain activity after ACL reconstruction during force control. J Orthop Res. 2011;29(9):1383-1389.

30. Baumeister J, Reinecke K, Weiss M. Changed cortical activity after anterior cruciate ligament reconstruction in a joint position paradigm: an EEG study. Scand J Med Sci Sports. 2008;18(4):473-484.

31. Courtney CA, Rine RM. Central somatosensory changes associated with improved dynamic balance in subjects with anterior cruciate ligament deficiency. Gait Posture. 2006;24(2):190-195.

32. Leeuw M, Goossens ME, Linton SJ, Crombez G, Boersma K, Vlaeyen JW. The fear-avoidance model of musculoskeletal pain: current state of scientific evidence. J Behav Med. 2007;30(1):77-94.

33. Chmielewski TL, Zeppieri G, Jr., Lentz TA, et al. Longitudinal changes in psychosocial factors and their association with knee pain and function after anterior cruciate ligament reconstruction. Phys Ther. 2011;91(9):1355-1366.

34. Fitts PM, Possner MI. Human performance. Oxford, England: Brooks and Cole; 1967.

35. Wulf G, Hoss M, Prinz W. Instructions for Motor Learning: Differential Effects of Internal Versus External Focus of Attention. J Mot Behav. 1998;30(2):169-179.

36. Durham K, Van Vliet PM, Badger F, Sackley C. Use of information feedback and attentional focus of feedback in treating the person with a hemiplegic arm. Physiother Res Int. 2009;14(2):77-90.

37. Lohse KR, Sherwood DE. Thinking about muscles: The neuromuscular effects of attentional focus on accuracy and fatigue. Acta Psychol. 2012;140(3):236-245.

38. Risberg MA, Holm I. The Long-term Effect of 2 Postoperative Rehabilitation Programs After Anterior Cruciate Ligament Reconstruction A Randomized Controlled Clinical Trial With 2 Years of Follow-Up. Am J Sports Med. 2009;37(10):1958-1966.

39. Wulf G, Lewthwaite R. Effortless motor learning? An external focus of attention enhances movement effectiveness and efficiency. 2010. Cambridge, MA: MIT Press.

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40. Chiviacowsky S, Wulf G. Self-controlled feedback: does it enhance learning because performers get feedback when they need it? Res Q Exerc Sport. 2002;73(4):408-415.

41. Sarter M, Gehring WJ, Kozak R. More attention must be paid: the neurobiology of attentional effort. Brain Res Rev. 2006;51(2):145-160.

42. Salmoni AW, Schmidt RA, Walter CB. Knowledge of results and motor learning: a review and critical reappraisal. Psychol Bull. 1984;95(3):355-386.

43. Shea CH, Wulf G, Whitacre C. Enhancing Training Efficiency and Effectiveness Through the Use of Dyad Training. J Mot Behav. 1999;31(2):119-125.

44. Wulf G, McConnel N, Gartner M, Schwarz A. Enhancing the learning of sport skills through external-focus feedback. J Mot Behav. 2002;34(2):171-182.

45. Wulf G, Chiviacowsky S, Schiller E, Avila LT. Frequent external-focus feedback enhances motor learning. Front Psychol. 2010;1:190.

46. Chiviacowsky S, Wulf G. Self-controlled feedback is effective if it is based on the learner’s performance. Res Q Exerc Sport. 2005;76(1):42-48.

47. Chiviacowsky S, Wulf G, Lewthwaite R. Self-controlled learning: the importance of protecting perceptions of competence. Front Psychol. 2012;3:458.

48. Wulf G, Shea C, Lewthwaite R. Motor skill learning and performance: a review of influential factors. Med Educ. 2010;44(1):75-84.

49. Wulf G, Chiviacowsky S, Lewthwaite R. Altering mindset can enhance motor learning in older adults. Psychol Aging. 2011;27(1):14-21.

50. Chiviacowsky S, Wulf G. Feedback after good trials enhances learning. Res Q Exerc Sport. Mar 2007;78(2):40-47.

51. Wulf G. Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc Psychol. 2013:6(1):77-104.

52. Badami R, VaezMousavi M, Wulf G, Namazizadeh M. Feedback after good versus poor trials affects intrinsic motivation. Res Q Exerc Sport. 2011;82(2):360-364.

53. Ahlden M, Samuelsson K, Sernert N, Forssblad M, Karlsson J, Kartus J. The Swedish National Anterior Cruciate Ligament Register: a report on baseline variables and outcomes of surgery for almost 18,000 patients. Am J Sports Med. 2012;40(10):2230-2235.

54. Sward P, Kostogiannis I, Roos H. Risk factors for a contralateral anterior cruciate ligament injury. Knee Surg Sports Traumatol Arthrosc. 2010;18(3):277-291.

Acknowledgment

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Dit proefschrift is eindelijk af en heeft langer geduurd dan het gemiddelde promotietraject. Maar zoals in goed Cruijffiaans: “Ieder nadeel heb zijn voordeel” - en dat is zeker ook van toepassing op mij. Een periode van ongeveer tien jaar heeft mij gevormd van een clinicus met vele academische vragen tot een beginnend academicus die ontwikkelde wetenschappelijke kennis graag wil toepassen en toetsen in de praktijk.

Graag wil ik alle mensen bedanken die de totstandkoming van dit proefschrift mogelijk hebben gemaakt. Mijn dankwoord schrijf ik min of meer in de chronologische volgorde waarin dit proefschrift tot stand is gekomen.

Lieber Dr. Thomas Schmalz, im Labor bei Otto Bock in Göttingen haben wir gemeinsam in unserer Freizeit erstmals Ganganalysen bei Patienten nach vorderer Kreuzbandläsion durchgeführt, wodurch mein Interesse an der Forschung geweckt wurde.

Prof. dr. P.U. Dijkstra, beste Pieter, ik heb in jou altijd een steun en toeverlaat gevonden. Ik vergeet nooit de eerste ontmoeting: een kleine kamer op C3 en jij, die met een van je vele messen een appel zat te schillen. Ondanks de gevaarlijke aanblik ben je een van de vriendelijkste mensen die ik ken. Hartelijk dank voor hulp bij de vele epidemiologische vragen waarop jij het antwoord wist. Je hebt mij enorm veel bijgebracht over de basisprincipes van wetenschap.

Prof. dr. J. Geertzen, beste Jan, hartelijk dank dat je me binnen vijf minuten doorstuurde om een afspraak te maken met Prof. dr. K. Postema. Dat was de eigenlijke start van mijn promotietraject. Korter en krachtiger had je me niet op weg kunnen helpen.

Prof. dr. K. Postema, beste Klaas, je was erg enthousiast (later ook nog gelukkig !) toen je mijn ideeën hoorde, maar stuurde me eerst weg met een opdracht: “Maak een literatuuroverzicht over het effect van braces bij patiënten met een voorste kruisbandlaesie. Als je dat af hebt, praten we verder.” Blijkbaar zag je het zitten want je zorgde voor een 0,2 fte aanstelling, wat me in staat stelde te starten met mijn promotieonderzoek. Hartelijk dank daarvoor. Je enthousiasme bij de overlegmomenten werkte inspirerend.

Dr. ir. A.L. Hof, beste At, een alom gerespecteerd wetenschapper en bovenal zeer bescheiden mens met af en toe vlijmscherpe humor. Ik ben trots en blij dat ik met je heb mogen samenwerken aan mijn eerste onderzoek.

Dr. M.P. Arnold, beste Markus, je kwam kijken bij de metingen die ik deed met ‘jouw’ patiënten. Er zijn maar weinig orthopeden die verder kijken dan het chirurgische trucje, maar ook op privévlak kan ik het goed met je vinden, mede dankzij onze voorliefde voor snelle auto’s. De rit in de Ford Mustang cabrio op Hawaï is onvergetelijk.

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Prof. dr. E. Otten, beste Bert, in februari 2005 stelde je voor mij de cruciale vraag: “Alli, begrijp je de mechanismen van je onderzoeksgegevens die je tot nu toe hebt vergaard?”. Het antwoord moest ik je natuurlijk schuldig blijven. Voor veel wetenschappelijke vraagstukken ben ik bij je geweest en elke keer kwam ik met nieuwe energie en ideeën weer terug op mijn kamer. Ik heb enorm veel kunnen leren van jouw unieke benadering van de wetenschap, je indrukwekkende kennis en analytisch vermogen en zie dit als een van de belangrijkste bijdragen aan mijn academische ontwikkeling. Op deze weg ga ik graag met je verder en we hebben al weer enkele interessante projecten gepland met studenten en promovendi.

Ronald Davidsz, hoewel je niet direct betrokken was bij mijn promotie, heb je toch een belangrijke rol gespeeld. Je hebt me talloze keren geholpen met je enorme kennis op het gebied van hardware en software. Ik mis je humor en ja, je mag de TopGear-tijdschriften houden.

Ook een dankwoord aan Dr. J. P. K. Halbertsma, beste Jan, dank voor de vele gevarieerde gesprekken en discussies die we op onze kamer voerden.

Tevens wil ik Helco van Keeken, Jos van Raaij en Hans Burgerhof danken voor hun expertise tijdens het laatste deel van mijn promotietraject.

Daarnaast wil ik nog een aantal mensen bedanken die een belangrijke rol in mijn academische ontwikkeling hebben gespeeld.

Prof. dr. J. Freiwald, lieber Jürgen, Du hast mich bei deinem Vortrag in Tucson inspiriert. Die Frage, ob die Quadrizepskraft immer 1:1 in Relation zur Funktion steht, hat mich sehr beschäftigt. Mittlerweile ist klar geworden, das dies nicht der Fall ist. Seit wir uns kennen, haben wir leider noch immer nicht die Zeit gefunden, uns auch mehr im privaten Bereich zu sehen.

P.D. Dr. M. Engelhardt, lieber Martin, wir kennen uns nun seit 2003 und es ist Dir zu verdanken, dass ich mich bei den zahlreichen Vorträgen und von Dir organisierten Symposien akademisch weiterentwickeln konnte. Ich danke Dir dafür und das Du mich bei der Gesellschaft für Orthopädisch-Traumatologische Sportmedizin (GOTS) eingebunden hast und ich mich dort sehr respektiert fühle.

Een dankwoord gaat uit naar Joep van der Harst, Alieke Drok en Marscha Bisschop die een wezenlijke bijdrage hebben geleverd aan de totstandkoming van dit proefschrift in het kader van hun studie Bewegingswetenschappen.

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Deze promotie had vanzelfsprekend niet tot stand kunnen komen zonder een kritische beooerdeling van het proefschrift en ik wil dan ook de leden van de leescommissie, prof. dr. R.L. Diercks, prof. L.H.V. van der Woude en prof. dr. J. Duysens hiervoor hartelijk bedanken.

Mijn ouders, dank jullie wel dat jullie mij het goede voorbeeld hebben gegeven waaruit ik heb geleerd dat je met hard werken ver kan komen.

Lieve Anne, zonder jou was het zeker niet gelukt om dit project af te ronden. Je hebt talloze keren mijn drafts voor artikelen gecorrigereerd. Ontzettend bedankt voor al je inbreng. Jij bent iemand op wie je altijd kunt bouwen. Op naar quality time.

Lieve Barbara, we hebben meer dan 20 jaar lief en leed gedeeld en 2 fantastische kinderen op de wereld gezet.

Gianna en Jacqueline, ik zal ook in de toekomst nog steeds op de bank zitten met mijn MacBook op schoot, maar ik ga zeker meer tijd vrijmaken voor leuke dingen samen met jullie.

Alli Gokeler

About the Author

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Alli Gokeler was born on 18 September 1967 in Groningen, the Netherlands. He obtained his degree in Physical Therapy in 1990 from the Rijkshogeschool Groningen. From 1991-2001 he worked as a physical therapist in the United States and Germany. Upon return to the Netherlands, he obtained a degree in Sports Physical Therapy from the Utrecht University of Applied Science in 2003. In 2005 he started on his PhD project at the University Medical Center Groningen, Center for Rehabilitation. Alli has a special interest in motor control after ACL injuries. His academic goal is to pursue a post-doc track to improve on his theoretical and practical competencies in research methods in human movement science with a special focus on development of prevention programs designed to reduce incidence of ACL (second) injury rate and associated occurrence of osteoarthritis.

H O N O R S A N D AWA R D S

2013 Third Price Jöllenbeck T, Freiwald J, Dann K, Gokeler A, Zantop T, Seil R, Miltner O. Paper of Highest Public Interest. GOTS Society for Orthopaedic Traumatologic Sports Medicine. Prevention of ACL Injuries. Review of Strategies and Evidence 2005 First Price Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K. Best Poster Award. GOTS Society for Orthopaedic Traumatologic Sports Medicine. An electromyographic analysis of landing strategies after ACL reconstruction. Munich, Germany2003 Second Price Benjaminse A, Gokeler A, van der Schans C. Student research award. Clinical Diagnosis of Anterior Cruciate Ligament Rupture. A Meta-Analysis. Royal Dutch Society for Physical Therapy, the Hague, the Netherlands

P E E R R E V I E W E D P U B L I C AT I O N S A C L

Baumgart C, Gokeler A, Donath L, Hoppe MW, Freiwald J. Effects of Static Stretching and Playing Soccer on Knee Laxity. Accepted Clin J Sports Med 2014.

Benjaminse A, Gokeler A, Dowling AV, Faigenbaum A, Ford KR, Hewett TE, Onate JA, Otten E, Myer GD. Optimization of the ACL Injury Prevention Paradigm: Novel Feedback Techniques to Enhance Motor Learning and Reduce Injury Risk Deficits. Accepted J Orth Sports Phys Ther 2014

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Gokeler A, Eppinga P, Dijkstra PU, Welling W, Padua DA, Otten E, Benjaminse A. Effect of Fatigue on Landing Performance Assessed with the Landing Error Scoring System (LESS) in Patients after ACL Reconstruction. A Pilot Study. Int J Sports Phys Ther. 2014;9(3):302-11.

Gokeler A, Benjaminse A, Welling W, Alferink M, Eppinga P, Otten B. The Effects of Attentional Focus on Jump Performance and Knee Joint Kinematics in Patients after ACL Reconstruction. Phys Ther Sport. 2014 doi: 10.1016/j.ptsp.2014.06.002.

Gokeler A, Bisschop M, Myer GD, Benjaminse A, Dijkstra PU, van Keeken HG, van Raay JJ, Burgerhof JG, Otten E. Immersive Virtual Reality Improves Movement Patterns in Patients after ACL Reconstruction: Implications for Enhance Criteria-based return-to-sport Rehabilitation. Knee Surg Sports Traumatol Arthrosc. 2014 doi.org/10.1007/s00167-014-3374-x.

Benjaminse A, Welling W, Otten B, Gokeler A. Novel Methods of Instruction in ACL Injury Prevention Programs. A Systematic Review. Phys Ther Sport. 2014. doi:10.1016/j.ptsp.2014.06.003.

Gokeler A, Bisschop M, Benjaminse A, Myer GD, Eppinga P, Otten E. Quadriceps Function Following ACL Reconstruction and Rehabilitation: Implications for Optimisation of Current Practices. Knee Surg Sports Traumatol Arthrosc. 2014;22(5):1163-74.

Gokeler A, Benjaminse A, van Eck CF, Webster KE, Schot L, Otten E. Return of Normal Gait as an Outcome Measurement in ACL Reconstructed Patients. A Systematic Review. Int J Sports Phys Ther. 2013;8(4):441-51.

Gokeler A, Benjaminse A, Hewett TE, Paterno MV, Ford KR, Otten E, Myer GD. Feedback Techniques to Target Functional Deficits Following ACL Reconstruction: Implications for Motor Control and Reduction of Second Injury Risk. Sports Med. 2013;43(11):1065-74.

Gokeler A, Benjaminse A, Hewett TE, Lephart SM, Engebretsen L, Ageberg E, Engelhardt M, Arnold MP, Postema K, Otten E, Dijkstra PU. Proprioceptive Deficits after ACL Injury: Are They Clinically Relevant? Br J Sports Med. 2012;46(3):180-92.

Benjaminse A, Gokeler A, Fleisig GS, Sell TC, Otten B. What is the True Evidence for Gender-related Differences During Plant and Cut Maneuvers? A systematic review. Knee Surg Sports Traumatol Arthrosc. 2011;19(1):42-54.

Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten E. Abnormal Landing Strategies after ACL Reconstruction. Scand J Med Sci Sports. 2010; 20(1):e12-9

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van der Harst JJ, Gokeler A, Hof AL. Leg Kinematics and Kinetics in Landing From a Single-leg Hop for Distance. A Comparison Between Dominant and Non-dominant leg. Clin Biomech. 2007;22(6):674-80.

Benjaminse A, Gokeler A, van der Schans CP. Clinical Diagnosis of an Anterior Cruciate Ligament Rupture: A Meta-analysis. J Orthop Sports Phys Ther. 2006;36(5):267-88.

Gokeler A, Schmalz T, Knopf E, Freiwald J, Blumentritt S. The Relationship Between Isokinetic Quadriceps Strength and Laxity on Gait Analysis Parameters in Anterior Cruciate Ligament Reconstructed Knees. Knee Surg Sports Traumatol Arthrosc. 2003;11(6):372-8.

P R E S E N TAT I O N S I N V I T E D S P E A K E R

Gokeler A, Benjaminse A, Padua D, Welling W, Alferink M, Otten E. Return to Sport” Wissenschaft und Anwendung für die Praxis. 7th Osnabrücker Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Osnabrück, Germany, March 2014

Gokeler A, Schmitt H, Züst P, Freiwald J, Fuhrmann R, Knupp M, Schueller-Weidekamm C, Hintermann B, Valderrabano V. 28th GOTS Society for Orthopaedic Traumatologic Sports Medicine Annual Meeting. Return to Sports after Ankle Injury. Mannheim, Germany, June 2013

Gokeler A, Benjaminse A, Eppinga P, Otten E. Rehabilitation after RTC repair and capsulolabral reconstruction. 6th Osnabrücker Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Osnabrück, Germany, March 2013

Gokeler A, Benjaminse A, Myer G, Wulf G. Novel Motor Leaning to Enhance Movement Patterns Prior Return to Sport after Anterior Cruciate Ligament Reconstruction. DGSP October 2012, Berlin, Germany

Gokeler A, Benjaminse A, Eppinga P, Otten E. Rehabilitation after ACL-Reconstruction. 5th Osnabrücker Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Osnabrück, Germany, March 2012

Gokeler A., Benjaminse A, Eppinga P, Otten E. New trends in ACL Rehabilitation. ELANN Symposium State of the Art in ACL Reconstruction and Rehabilitation, Groningen, the Netherlands. December 2011

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Otten E, Benjaminse A, Gokeler A. Synthese van het Onderzoek naar Leren, Cognitie en Gedrag bij Preventie en Herstel na (Knie) Blessure. 9e Groningen Sports Medicine Symposium 2011. Groningen, the Netherlands. January 21, 2011

Gokeler A. Sports Medicine Symposium, University of Regensburg. Patellofemoral disorders. What’s the Evidence ? Regensburg, November 2010

Gokeler A. GOTS Society for Orthopaedic Traumatologic Sports Medicine. ACL Expert Meeting. Berlin, Germany, May 2010

Gokeler A, Lehmann M. 3rd Osnabrücker Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Rehabilitation after Rotator Cuff Repair. Osnabrück, Germany, March 2010

Gokeler A, Lehmann M. 71st German Orthopaedics and Traumatology International Meeting. Update on Surgical treatment SLAP Lesions. Berlin, Germany, October 2009

Gokeler A. Royal Dutch Society for Physical Therapy RGF Symposium “Shaky Knees”. ACL-Reconstruction - Good Hardware and/or Software ? Heerenveen, the Netherlands, March 2009

Gokeler A, Lehmann M. Athletikum Group Update 2008. 2nd Interdisciplinary Symposium of the Shoulder and Hip. Rehabilitation Following Arthroscopic Shoulder Stabilization. Freiburg, Germany, November 2008

Gokeler A, Lehmann M. 1st Freiburger Shoulder Symposium. Rehabilitation of the Shoulder. Freiburg, Germany, November 2007

Gokeler A, Otten E. Dutch Society for Sports Medicine Symposium. Residual deficits after ACL-Reconstruction. Wijk aan Zee, the Netherlands, November 2007

Gokeler A, Engelhardt M, Freiwald J. 22th GOTS Society for Orthopaedic Traumatologic Sports Medicine Annual Meeting. Instructional Course: Rehabilitation after ACL-Reconstruction. Munich, Germany, June 2007

Gokeler A, Engelhardt M. 13th German Society for Foot and Ankle Annual Meeting. Instructional Course: Rehabilitation After Inversion Trauma of the Ankle. Bielefeld, Germany, March 2007

Gokeler A, Engelhardt M, Freiwald J. International GOTS Society for Orthopaedic Traumatologic Sports Symposium: “Around the Knee“: Rehablilitation after ACL-Reconstruction. Florence, Italy, September 2006

Gokeler A, Engelhardt M, Freiwald J. 14th International Sports Medicine Symposium Soccer World Championships “Around the Ball”: Rehabilitation after Inversion Trauma of the Ankle. Frankfurt, Germany, May 2006

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Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten. Dutch Society Sports Physiotherapy. “A leg to stand on”: Pre-activation of leg muscles during single leg hop test after ACL-Reconstruction. Nieuwegein, the Netherlands, April 2006

Gokeler A, Engelhardt M, Freiwald J. 4th Bielefelder Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Rehabilitation after Total Knee Prosthesis. Bielefeld, Germany, March 2006

Gokeler A, Engelhardt M, Freiwald J. 7th German Society Sports Medicine section Biomechanics, Motor Control and Exercise “Prevention and Rehabilitation”: Biomechanical Analysis after ACL-Reconstruction. Bad Sassendorf, Germany, February 2006

Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K. 2nd German Symposium Research in Physical Therapy. Landing strategies after ACL-Reconstruction. An Electromyographic Analysis. Göttingen, Germany, September 2005

Gokeler A, Engelhardt M.1st Kieler Sports Medicine Symposium. Muscle Injuries in Endurance Sports, Kiel, Germany, August 2005

Gokeler A, Engelhardt M, Freiwald J. 20th.GOTS Society for Orthopaedic Traumatologic Sports Medicine Annual Meeting. Instructional Course: Neuromuscular Changes after Knee Injuries. Munich, Germany, June 2005

Gokeler A, Lehmann M, Engelhardt M, Freiwald J. 3rd Bielefelder Symposium State of the Art in Orthopaedics, Traumatologie and Physical Therapy. Rehabilitation after Shoulder Stabilization. Bielefeld, Germany, March 2005

S C I E N T I F I C P L AT F O R M P R E S E N TAT I O N S

Gokeler A, Benjaminse A, Welling W, Alferink M, Otten E. Effect of Verbal Feedback Instructions on Landing Mechanics in Patients after ACL Reconstruction. ACL Study Group Meeting. Cape Town, South Africa, January 26-30, 2014

Gokeler A, Bisschop M, Keeken, van HG, Burgerhof JH, Raaij JJAM, Otten E. Cognitieve Veranderingen in de Motorische Controle na een Voorste Kruisbandreconstructie. Voorjaarcongres Dutch Orthopedic Society, Utrecht, May 31, 2013

Benjaminse A, Gokeler A, Cortes N, Otten, E. Effects of Stiff and Soft Landing Techniques on Knee Loading during a Single-Leg Cross-Over Hop. ACL Research Retreat V. Greensboro, NC, USA. March 22-24, 2012

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Gokeler A, Bisschop M, Benjaminse A, Eppinga P, Arnold M, Otten E. The Quadriceps Muscle Weakness Enigma after ACL-reconstruction. ACL Study Group Meeting. Jackson Hole, WY, USA. February 12-17, 2012

Benjaminse A, Gokeler A, Fleisig GS, Otten E: What is the True Evidence for Gender Related Differences in ACL Injury During Plant and Cut Maneuvers? A Systematic Review. ESSKA Meeting. Oslo, June 2010

Gokeler A, Benjaminse A, Ageberg E, Engebretsen L, Engelhardt M, Arnold M, Postema K, Otten E, Dijkstra P. ACL Study Group Meeting. Proprioceptive Deficits after ACL-injury. Are They Clinically Relevant ? A Systematic Review. Phuket, Thailand, 20-26 February 2010

Benjaminse A, Gokeler A, Schans C van der. Clinical Diagnosis of Anterior Cruciate Ligament Rupture. A Meta-Analysis. GOTS Society for Orthopaedic Traumatologic Sports Medicine Annual Meeting. Munich, Germany, June 2007

Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K, Otten. Congress on Sport Rehabilitation and Traumatology Health, Prevention and Rehabilitation in Soccer. Abnormal landing strategies after ACL-Reconstruction. Milan, Italy, April 2007

Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K. 12th ESSKA 2000 Congress. Landing strategies after ACL reconstruction. An electromyographic analysis. Innsbruck, Austria, May 2006

Gokeler A, Hof AL, Arnold MP, Dijkstra PU, Postema K. ACL Study Group Meeting. Landing strategies after ACL reconstruction. An Electromyographic Analysis. Hawaii, March 2006

Gokeler A, Lehmann M, Schmidt-Wiethoff R. 20th GOTS Society for Orthopaedic Traumatologic Sports Medicine Annual Meeting. Role of the Scapula in Shoulder Instability. Munich, Germany, June 2005.

Gokeler A, Lehmann M, Schmidt-Wiethoff R. 12th German Shoulder and Elbow Society Annual Meeting. Role of the Scapula in Shoulder Instability. Weimar, Germany, May 2005

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T H E S I S M E N TO R I N G

Welling W., Benjaminse A, Gokeler A, Otten E. Systematic review effect of attentional focus after ACLR. University Medical Center Groningen, Center for Human Movement Science. University Groningen, the Netherlands.

Schot L. A.Gokeler, E. Otten.Use of the CAREN system University Medical Center Groningen, Center for Human Movement Science. University Groningen, the Netherlands.

Bisschop M, A. Gokeler, Benjaminse A, P.Eppinga, Otten E. Systematic Review Evidence of Effectiveness Rehabilitation after ACL Reconsctruction. Center for Human Movement Science. University Groningen, the Netherlands.

Benjaminse A, Gokeler A, Schans C van der. Clinical Diagnosis of Anterior Cruciate Ligament Rupture. A Meta-Analysis. Hanze University Applied Sciences, Department of Physical Therapy Groningen, the Netherlands.

R E V I E W E R

American Journal of Sports MedicineClinical BiomechanicsMedicine and Science in Sports and ExerciseKnee Surgery Sports Traumatology Arthroscopy Journal of Athletic TrainingJournal of Sport Rehabilitation European Journal of Applied Physiology

M E M B E R S H I P S

ESSKA ACL Study Group GOTS Society for Orthopaedic Traumatologic Sports MedicineKNGF: Royal Dutch Society for Physical Therapy, Section Sports Physical Therapy

Financial Support

Financial Support

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W E T E N S C H A P P E L I J K O N D E R Z O E K A F D E L I N G R E VA L I D AT I E G E N E E S K U N D E – C E N T R U M V O O R R E VA L I D AT I E U M C G

EXPANDExtremities, Pain and Disability

Missie: EXPAND draagt bij aan participatie en kwaliteit van leven van mensen met aandoeningen en amputaties van de extremiteiten of met pijn aan het bewegingsapparaat.

EXPAND omvat twee speerpunten: onderzoek naar aandoeningen aan en amputaties van extremiteiten met nadruk op stoornissen, activiteiten en participatie en onderzoek naar chronische pijn en arbeidsparticipatie. EXPAND draagt bij aan het UMCG-brede thema Healthy Ageing.

Research Department of Rehabilitation Medicine – Center for Rehabilitation UMCG

EXPANDExtremities, Pain and Disability

Mission: EXPAND contributes to participation and quality of life of people with conditions and amputations of the extremities and musculoskeletal pain.EXPAND focuses on two spearheads: research on the conditions and amputations of the extremities with emphasis on body functions and structures, activities and participations, and chronic pain and work participation. EXPAND contributes to Healthy Aging, the focus of the UMCG.

Financial support for the research and printing of the dissertation in fulfillment of the requirements for the degree of doctor of philosophy was provided by:

University of Groningen, University Medical Center Groningen, Center for Rehabilitation

School of Behavioral and Cognitive Neurosciences (BCN), University of Groningen

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Printing of this dissertation was financially supported by: