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Effect of skin movement artifact on knee kinematics during gait and cutting motions measured in vivo
Gait & Posture 24 (2006) 152–164 www.elsevier.com/locate/gaitpost
Effect of skin movement artifact on knee kinematics during gait and cutting motions measured in vivo Daniel L. Benoit a,b,c,*, Dan K. Ramsey d, Mario Lamontagne f,g, Lanyi Xu f, Per Wretenberg b,e, Per Renstro¨m a,b a
Institution for Surgical Sciences, Section of Sports Medicine, Karolinska Institute, Stockholm, Sweden b Department of Orthopaedics, Karolinska Hospital, Stockholm, Sweden c Department of Mechanical Engineering, University of Delaware, 106 Spencer Lab, Newark, DE 19711, USA d Department of Physical Therapy, University of Delaware, Newark, DE, USA e Institution for Surgical Sciences, Section of Orthopaedics, Karolinska Institute, Stockholm, Sweden f School of Human Kinetics, University of Ottawa, Ottawa, Canada g Department of Mechanical Engineering, University of Ottawa, Ottawa, Canada Received 6 November 2004; received in revised form 25 March 2005; accepted 9 April 2005
Abstract Eight healthy male subjects had intra-cortical bone-pins inserted into the proximal tibia and distal femur. Three reflective markers were attached to each bone-pin and four reflective markers were mounted on the skin of the tibia and thigh, respectively. Roentgenstereophotogrammetric analysis (RSA) was used to determine the anatomical reference frame of the tibia and femur. Knee joint motion was recorded during walking and cutting using infrared cameras sampling at 120 Hz. The kinematics derived from the bone-pin markers were compared with that of the skin-markers. Average rotational errors of up to 4.48 and 13.18 and translational errors of up to 13.0 and 16.1 mm were noted for the walk and cut, respectively. Although skin-marker derived kinematics could provide repeatable results this was not representative of the motion of the underlying bones. A standard error of measurement is proposed for the reporting of 3D knee joint kinematics. # 2005 Elsevier B.V. All rights reserved. Keywords: Soft tissue artifacts; Movement analysis; In vivo; Three-dimensional analysis; Knee joint
1. Introduction One of the most common methods to measure knee joint motion is to track the motion of clusters of three or more retro-reflective or light emitting markers affixed to the skin of the shank and thigh. The marker configurations used may influence the accuracy of the reconstructed data [1]. However, other factors may play a more significant role in determining the validity of the results. When applied to measuring knee joint kinematics based on the position of the tibia and femur, the accuracy of these measurements is prone * Corresponding author at: Department of Mechanical Engineering, University of Delaware, Spencer Labs 126, Newark, DE 19716, USA. Tel.: +1 302 831 2410/2423; fax: +1 302 831 3466/3619. E-mail address: [email protected] (D.L. Benoit). 0966-6362/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2005.04.012
to error due to skin movement artifact [2]. A recent review by Leardini et al. [3] identifies that previous investigations have been lacking in sample size [4], or have had methodological limitations [5,6]. While only three and two subjects were evaluated in these studies, respectively, the lack of agreement between the shape of the kinematic profiles derived from the skin- and pin-markers poses an important question as to how well skin-marker kinematic profiles represent the underlying bones. Others have used different techniques to quantify movement artifact on the shank and thigh [2] but the subjects investigated were from a population recovering from leg fractures. In addition, only two subjects were available with thigh mounted pin-markers and no subjects were simultaneously instrumented with pin-markers on both the shank and thigh. Recent progress using a 250 frame/s
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stereoradiographic system is encouraging [7] but the confined area of measurement limits the movement possibilities of the subject. Ideally, kinematic data would be reported with a standard error of measurement that reflects the uncertainty of the reported findings caused by this skin movement artifact inherent in the measurement technique. When comparing two groups of subjects and attempting to detect kinematic differences associated with a population difference the findings could be confidently reported with the knowledge that observed differences are due to the population differences and not measurement error. Tracking the motion of the tibia and femur with surgically implanted intra-cortical bone-pins instrumented with clusters of markers is an accurate means of directly measuring skeletal motion under physiologically relevant testing conditions [8]. Target clusters are tracked using any one of the commercially available motion analysis systems and movement of the underlying bones can be derived. The use of percutaneous bone-pins mounted in the tibia and femur and instrumented with no less than three reflective markers can provide rigid body reconstruction using motion analysis. Roentgen-stereophotogrammetric analysis (RSA) has been used to relate the position of these markers to the anatomical reference frame and to derive an anatomical coordinate system to describe motion [9]. The principal is to reconstruct the position of the bone-embedded markers to an anatomical reference point, such as the deepest point of the intercondylar groove for the femur and the most proximal point of the medial condylar eminence for the tibia [4,5]. The anatomical reference points are used to determine the origin of each segment, respectively. Using RSA it is possible to apply a bone-embedded, or anatomical, reference system when describing joint motion in a laboratory reference frame. This simplifies data interpretation and, given an accurate and reproducible choice of anatomical reference points and coordinate system alignment, allows comparisons not only within subjects but also potentially across subjects. Combining RSA with bone-pins allows an accurate representation of the bones but is technically difficult and invasive [10,11]. However, the advantages include the ability to accurately represent tibio-femoral kinematics and, although an invasive technique, subjects have been shown to walk [5,6,9,12], run [4,9,13] and hop [5] normally. Knowledge of non-sagittal plane tibio-femoral kinematics is necessary if we are to improve our knowledge of the mechanisms associated with knee joint injury and the progression of knee joint degeneration. For example, the anterior cruciate ligament (ACL) injury is believed to lead to degenerative joint disease [14]. Since injury mechanisms of the ACL are thought to combine tibio-femoral rotation with anterior tibial translation [15], knowledge of combined sagittal and non-sagittal plane tibio-femoral joint motion under physiological conditions is essential for detecting critical phases of motion that may predispose the ACL to
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loading. To our knowledge there is no information in the literature about the ability to accurately measure tibiofemoral joint motion in non-sagittal plane movements. This lack of information seriously limits the ability to investigate knee joint injury mechanisms using non-invasive techniques. The purpose of this investigation is to quantify the error caused by skin movement artifact when reporting the kinematics of the tibio-femoral joint during movements that incorporate sagittal and non-sagittal plane rotations. We hypothesise that skin movement error will reduce the ability to accurately measure 3D tibio-femoral kinematics and that non-sagittal plane movements will be most affected by skin movement artifact.
2. Methods 2.1. Subjects Eight healthy, moderately active, male subjects with no history of knee injury or prior surgical treatment of the lower limbs were studied (Table 1). Informed consent was obtained from the subjects and the study was approved by the Ethics Committee of the Karolinska Hospital, Stockholm, Sweden. 2.2. Surgical procedure Stainless steel Apex self-drilling/self-tapping pins (Stryker Howmedica AB Sweden, 3.0 mm diameter, #5038-2110) were inserted under local anaesthetic into the distal femur and proximal tibia of the right leg [11] at the Karolinska University Hospital (Stockholm, Sweden). The femoral pin was inserted between the Iliotibial (IT) band and the quadriceps tendon superior of the vastus lateralis to minimise impingement problems. Following surgery subjects performed active flexion and extension movements while standing to identify whether movement restrictions were evident. Subjects were then transported by wheelchair to the motion analysis laboratory for data collection. The pins remained inserted for the duration of the test. Upon
Table 1 Subject characteristics Subject
Age
Height (cm)
Weight (kg)
1 2 3 4 5 6 7 8
32 22 22 32 31 27 22 22
185 181 180 171 174 178 181 175
89 78 78 86 62 76 93 63
Average
26
178.1
78.1
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completion of the experiments (approximately 2 h), subjects returned to the operating theatre to have the dressing and pins removed. 2.3. Motion recordings
Fig. 1. (a) Picture of the bone-pin and surface marker configurations for a representative subject. Note: the pins are inserted in the tibia and femur, respectively. Each pin is instrumented with a target cluster, comprised of four reflective markers. The skin is instrumented with four reflective surface markers; (b) RSA procedure and calibration box. The right leg is extended
Triads of three non-collinear 7 mm reflective markers (pin-markers) were affixed to the pins. Additional clusters of four 10 mm surface markers (skin-markers) were affixed onto the lateral and frontal aspects of both the right thigh and shank (Fig. 1a and b). Skin-markers were spaced 10–15 cm from adjacent markers within their respective cluster and their arrangement was chosen to ensure they remained noncoplanar in at least two camera views throughout the range of motion. Reflective markers were also placed on the right heel, 5th metatarsal and lateral malleolus. Bone-pin and skin-marker trajectories were tracked within 0.8 m3 measurement volume (1.1 m 0.8 m 0.9 m) using four infrared cameras (ProReflex, Qualisys AB, Sweden), sampling at 120 Hz. Marker coordinates were transformed using the direct linear transform (DLT) and the raw 3D coordinates exported and saved to a local computer for analysis. The motion analysis system simultaneously collected both the skin- and pin-marker configurations for each standing and movement trial. Participants were asked to perform a series of normal walking trials and lateral cutting manoeuvres. Each subject was given several practice trials to familiarise themselves with the pins and testing protocol. Ground reaction forces (GRF) were measured simultaneously at 960 Hz using a Kistler force plate (Kistler Instruments AG, Winterhur, Switzerland) located midway through the measurement volume. For gait testing, subjects walked along a 12 m walkway at a selfselected pace. Contact with the force plate and no evidence of targeting were required for a trial to be considered. Before performing the lateral cutting manoeuvre, subjects jumped for maximal horizontal distance. Their longest measurement was recorded and marked on the floor to determine the proper takeoff distance to the force platform. From an initial standing position the subject pushed off using the left leg and, upon landing onto their right foot, immediately pushed off the platform, cutting to the left at an angle of approximately 458. Five measurement trials were recorded for each movement task as well as a standing reference trial before and after each block of movement trials. Subjects stood in a neutral position and were instructed to align their feet parallel to the force platform to define the tibial and femoral anatomical coordinate systems. The orientation of the target clusters from the first reference trial was matched against the second to verify the pins did not bend and the triad did not rotate during testing. through the box with the bone-pins and reflective markers in place. The knee is flexed between 08 and 108, RSA recordings were taken following motion analysis sessions.
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2.4. RSA technique and anatomical reference frame Following the motion analysis recordings, the leg was extended through a biplanar calibration box (Cage 10, RSA Biomedical Innovations, Umea˚, Sweden) and biplanar radiographs (RSA) were recorded (Fig. 1b). All radiographs were taken with the subject supine and the knee flexed between 08 and 108. From these radiographs, two local anatomical reference points were identified and digitised with the aid of an experienced RSA technician (Sahlgrenska University Hospital Gothenburg, Sweden; see acknowledgements). In total, 19 points were digitised to derive the anatomical reference system using UMRSA software (version 5, Biomedical Innovations-AB, Umea, Sweden). These included: 1–4. 5. 6. 7–8. 9.
10–14. 15.
16. 17–18. 19.
Tibial pin-markers. Proximal medial tibial eminence (tibial reference point). The most distal point along a line trough point 5 and parallel to the long axis of the tibia. Medial and lateral edges of proximal tibia respectfully. A distal point along a line drawn perpendicular to the long axis of the tibia and running originating at the tibial reference point. Femoral pin-markers. Proximal (deepest) point of the condylar groove (notch) (femoral reference point). The most distal point along a line trough point 15 and parallel to the long axis of the femur. Medial and lateral edges of the distal femur, respectively. A distal point along a line drawn perpendicular to the long axis of the femur and originating at the femoral reference point.
Zt
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vector joining points 5 and 6; from the tibial origin directed longitudinally along the tibial axis in the frontal plane.
2.5. Kinematic technique Custom written software (Matlab, Mathworks, USA) was developed and validated to process the 3D kinematic information derived from the bone-pins and surface markers, respectively [16]. The kinematic profile was described using the terminology and the ordered sequence of the Joint Coordinate System (JCS) [17]. In brief, the bone-embedded coordinate system is defined from the RSA coordinate data: the digitised points are used to locate the origin and direction of the anatomical reference frames. Transformation matrices for the pin-markers of both tibia and femur were derived to relate the position of these points to their respective anatomical origins [17,18]. 3D pin-marker coordinates from the standing reference trials (SRT) were used to determine the transformation matrix from the laboratory reference frame to the bone-embedded reference frame. This transformation matrix was then used to determine the location of the skin-markers with respect to the boneembedded reference frame (Fig. 2). Kinematic data for both the pin- and skin-markers were derived and low-passed filtered at 12 Hz using a 20th order FIR digital filter (Matlab). The cut-off frequency was determined by running a Fourier analysis that retained 95% of the original signal (both angular and linear data) and by visual inspection. The limited measurement volume allowed recording of a limited pre-foot-strike phase and complete stance phase of the walking and cutting movements. Foot-strike and toe-off were determined using the force platform data and the corresponding frame number was identified in the kinematic data. The kinematic data was normalised to 100% stance
The origin of the femoral reference frame was located at the deepest point of the intercondylar groove (point 15). The origin of the tibial reference frame was located at the highest point of the medial intercondylar eminence (point 5). Local coordinate systems of the femur and tibia were defined as follows: Xf Yf Zf
Xt Yt
cross product of vectors Zf and Yf; from the femoral origin, directed laterally. cross product of Zf and vector joining points 17 and 18; from the femoral origin, directed anteriorly. vector joining points 15 and 16; from the femoral origin directed longitudinally along the femoral axis in the frontal plane. cross product of vectors Zt and Yt; from the tibial origin, directed laterally. cross product of Zt and vector joining points 7 and 8; from the tibial origin, directed anteriorly.
Fig. 2. Schematic representation of the anatomical reference frames and the bone-pin marker cluster configurations. Adapted from Benoit DL (2005): motion analysis of the knee: kinematic artifacts, EMG normalisation and joint forces. Ph.D. thesis, Karolinska Institutet, Stockholm.
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phase (foot-strike to toe-off = 100%). Pre-foot-strike was expressed as a function of the normalised stance phase and ranges from 10% (or the longest duration of pre-foot-strike for that given subject) to 0% (foot-strike). 2.6. Statistical analysis Three points of interest during the stance phase of the walking and cutting cycle were chosen for statistical analysis: heel strike (HS); mid-stance point (corresponding with maximum knee flexion angle during the first 60% of stance) (MS); and toe-off (TO). The kinematic data derived from the bone-pins was considered the ‘gold standard’ of measurement. Paired, two-tailed Student’s ttests were used to determine if skin derived kinematics at the three time-points differed from those derived from the bone-pins. Kinematic data at HS, MS, TO are often extracted and used for comparisons of populations in gait studies. As we were interested in the validity of making such comparisons, we chose to treat each extracted point as independent. Accuracy of the skin-marker kinematics was calculated as the absolute difference between skin and pin knee flexion/extension, abduction/adduction and internal/external rotation angles and medio/lateral, antero/posterior and distraction/compression translations at HS, MS and TO. In addition, the standard error of estimate (S) was calculated for both walking and cutting. In this approach, the error is implicitly assumed to arise entirely from the skinmarker data (Y), while the pin-marker data (X) is assumed to be without error (E). In other words, since we assume that X for a given point in time is accurate, then Y will predict X such as (Y + E) within a certain confidence interval for that given time point (see Appendix A for a description of S). This data was calculated by comparing the pin- and skinmarker data across all subjects for each trial and at every time point, with the average calculated across time points (total number of time points: n = 110 walking, n = 105 cutting due to a shorter observed pre-foot-strike phase in some subjects).
3. Results Of the eight subjects, two subjects (numbers one and three in Table 1) had data that were not usable: one subject was excluded due to incomplete RSA data that rendered transformation impossible, while the second subject bent the femoral pin during knee flexion, the result of an interaction with the soft tissue and musculature. No subjects experienced significant pain and/or discomfort during the experiments and all reported being able to move their knee freely despite pin implantation. However, one subject was limited to three trials for both walking and cutting while another was limited to three trials for walking as recommended by the attending surgeon to reduce exposure time for these subjects. Simultaneously recorded high-speed digital video files (100 frames/s; JVC model DVL9000, Japan) of the motions indicated that all subjects contacted the force plate with the heel during walking and the mid-foot during cutting. Figs. 3 and 4 display rotations and translations of a representative subject during both walking and cutting, respectively. Absolute error between the skin-marker and pin-marker kinematics at heel strike, mid-stance and toe-off during the walking and cutting motions are noted in Table 2. A significant difference in reporting skin-marker derived kinematics with respect to actual tibio-femoral kinematics is evidenced at heel strike, mid-stance and toe-off for both walking and cutting rotations and translations. In the stance phase of walking the average rotational absolute error ranged from 2.48 to 4.48 while translational errors ranged from 3.3 to 13.0 mm. In the cutting movement the range of absolute errors and maximum absolute error were higher for both rotations (3.38 to 13.18) and translations (5.6 to 16.1 mm) respectively. The relationship between skin and pin derived kinematic profiles observed across subjects differed considerably. Figs. 5 and 6 illustrate the average error due to skin movement for each during the stance phase of walking and cutting, respectively. In Figs. 5 and 6 a positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-
Table 2 Absolute error values of skin-marker derived kinematics at three time points during walking and cutting of knee rotations and translations: flexion–extension (Flex/Ext), adduction–abduction (Add/Abd), internal–external rotation (Int/Ext); medio–lateral (Med/Lat), anterior–posterior (Ant/Post) and distraction– compression (Dist/Comp) Rotations (degrees S.D.) Flex/Ext
Add/Abd
Translations (mm S.D.) Int/Ext
Med/Lat
Ant/Post
Dist/Comp
Walk Foot-strike Mid-stance Toe-off
2.8 (2.6)a 2.4 (2.0)a 2.7 (2.4)
2.5 (2.7) 3.1 (3.3) 4.4 (3.2)a
2.8 (2.0)a 2.4 (1.1) 2.2 (2.1)
5.0 (2.6) 5.5 (3.1)a 8.0 (5.7)
7.7 (4.4)a 6.2 (5.4) 13.0(5.0)a
5.0 (2.9)a 3.3 (2.4)a 5.0 (2.5)a
Cut Foot-strike Mid-stance Toe-off
3.9 (2.9) 4.0 (2.5) 4.2 (2.7)
6.7 (5.4)a 5.9 (3.1)a 13.1 (9.8)
5.4 (4.2)a 5.4 (4.0)a 3.3 (1.8)a
7.3 (4.4) 5.9 (4.5)a 13.9(10.1)
5.6 (5.1)a 6.7 (4.4)a 16.1 (8.9)
6.3 (4.0)a 5.6 (3.8)a 8.3 (6.2)a
a
Significant difference between skin- and pin-marker data (two-tailed paired Student’s t-test, p < 0.05).
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Fig. 3. Walking trials of a representative subject, subject-4. Knee joint flexion (+)/extension () (Flex/Ext), adduction (+)/abduction () (Add/Abd) and internal (+)/external () (Int/Ext) rotation data is presented in the left column while lateral (+)/medial () (Med/Lat), anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp) are in the right column. Pin-marker labels are unfilled, skin-markers in bold.
marker derived knee joint rotations and translations. During walking (Fig. 5) there appears to be some agreement across subjects in the shape of the error profile for some rotations (flexion/extension; internal/external) and translations (anterior/posterior; distraction/compression). With respect to the
magnitude and direction of the error (over or under-estimation of joint position) there appears to be some agreement for distraction/compression. During cutting (Fig. 6) there appears to be greater agreement in the shape of the error curves for both rotations
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Fig. 4. Cut movement trials of a representative subject, subject-4. Knee joint flexion (+)/extension () (Flex/Ext), adduction (+)/abduction () (Add/Abd) and internal (+)/external () (Int/Ext) rotation data is presented in the left column while lateral (+)/medial () (Med/Lat), anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp) are in the right column. Pin-marker labels are unfilled, skin-markers in bold.
(adduction/abduction, internal/external rotation) and translations (lateral/medial; antero/posterior) while the magnitude and direction of the error (over or under-estimation of joint position) also shows agreement for distraction/ compression and antero/posterior translations. While the absolute error is the absolute difference between the skin-marker and pin-marker derived kinematics, the average standard error of the estimate (S)
describes the error associated with predicting pin-marker based tibio-femoral kinematics from skin-marker derived kinematics. The average S for walking and cutting movements is found in Table 3 and represents the expected margin of error when predicting tibio-femoral joint motion using skin-markers. These error values were higher in the cutting movement for both rotations and translations.
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Fig. 5. Progression of error due to skin movement during walking for all subjects. Figure show the average difference between skin-marker and pin-marker data for each subject as it progressive during stance. A positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-marker derived knee joint rotations and translations. Left column: knee joint flexion (+)/extension () (Flex/Ext); adduction (+)/ abduction () (Add/Abd) and internal (+)/external () (Int/Ext). Right column: lateral (+)/medial () (Med/Lat); anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp).
4. Discussion The purpose of this investigation was to quantify the error caused by skin movement artifact when reporting the kinematics of the tibio-femoral joint during movements that
incorporate sagittal and non-sagittal plane rotations. Skin movement artifact is inherent in motion analysis using surface markers and this study represents a comprehensive record of the effect of skin movement during gait in healthy subjects and, to our knowledge, the only record of the effect
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Fig. 6. Progression of error due to skin movement during cutting for all subjects. It shows the average difference between skin-marker and pin-marker data for each subject as it progressive during stance. A positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-marker derived knee joint rotations and translations. Left column: knee joint flexion (+)/extension () (Flex/Ext); adduction (+)/ abduction () (Add/Abd); internal (+)/external () (Int/Ext). Right column: lateral (+)/medial ()() (Med/Lat); anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp).
of skin movement during the cutting movement. We found within subject data to be repeatable when using either the skin or pin mounted markers for both the walk and cut. This was encouraging however as the error associated with skin movement artifact differed widely across subjects. Skin movement of the thigh and shank may be large enough to
mask the actual movements of the underlying bones, thus making reporting of knee joint kinematics using skinmarkers potentially uncertain. With three subjects Reinschmidt et al. [4] reported average errors relative to the range of motion of the knee during the stance phase of running of 21% (flexion/
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Table 3 Average standard error of the estimate (S) describing the error associated with predicting tibio-femoral kinematics from skin-marker derived kinematics Rotations (8)
Walk Cut
Translations (mm)
Flex/Ext
Add/Abd
Int/Ext
Med/Lat
Ant/Post
Dist/Comp
2.5 6.3
3.6 4.5
2.9 3.0
5.9 8.0
6.8 5.5
2.7 7.1
Average calculated for each data point of the stance phase (average of 110 data points) based on the estimated prediction of all walking (n = 25) and cutting (n = 28) trials. For a description of S see Appendix A.
extension), 63% (internal/external rotation) and 70% (abduction/adduction). No discussion of the error in recording joint translation was reported while an inadequate calibration area added 28 measurement error to the rotational data. Though only two subjects were observed over a limited stance time, Houck et al. [6] found absolute differences of up to 2.28 in the sagittal plane, 2.78 in the frontal plane and 1.88 in the transverse plane, while up to 13.9 mm of linear displacement was observed during walking. The results of these studies are comparable to those observed in our study. Comparing kinematic data collected simultaneously from surface markers and that of bone-embedded marker systems fixed to an external fixation device, Cappozzo et al. [2] reported skin-marker movement of 1–3 cm on the shank and thigh, respectively leading to slightly higher rotational errors then found in our study. However, the external fixator and the fracture suffered by the subjects may have affected the normal skin movement, walking ability and normal muscle mass of the test subjects. Using an externally fixed ‘bone tracker’ Manal et al. [1,19] found that linear translations of the knee joint using skin-markers of 2.1–7 mm depending on the plane of movement, with average rotation errors below 38. Individual subject deviations ranged between 48 and 78, depending on the skin-marker configuration. These observations were solely related to skin movement of the shank during the stance phase of walking. It can be reasoned that errors would likely have been higher had the effect of thigh skin movement also been measured however the fact that their results are comparable to our study shows promise for the use of less invasive techniques to track bone motion. With respect to walking, the profile of the error curves appears to be somewhat similar in flexion/extension, internal/ external rotation, anterior/posterior translation and distraction/compression. However, the direction of the error (over/ under-estimation) differs widely in magnitude. It seems that if the initial error could be estimated at a given time point (footstrike for example), the error could potentially be predicted for that subject and the aforementioned parameters. This however requires further investigation. The error of subject 5 during walking consistently differs from that of the other subjects around 60% of the stance phase. Using the marker tracking portion of the QTrac (Qualisys AB, Sweden) analysis software, visual inspection of this subject’s raw pin-marker data revealed that tibiofemoral motion did occur around this time point when visualised with the pin-markers. This movement pattern was
not witnessed using the skin-markers and thus contributed to the altered error pattern around this time point. We believe that the skin-markers were incapable of tracking this underlying motion, as it should have been simultaneously detected. The bone-pins and marker triad of this subject were not found to be damaged or loosened upon removal and this occurrence was not witnessed during the cutting trial, which was performed after the walking trials. We therefore believe this detected motion was a function of their walking style and anatomy. During the cut the profile of the error curves appears to be more consistent than during walking. While the error magnitudes are generally larger it appears that the skin moves in a more consistent pattern across subjects and indicates that the skin-markers were not sensitive enough to track the motions of the underlying bones for this more ballistic movement. The most important example is in the measure of anterior/posterior tibial translation where skinmarker kinematics would have indicated a posterior displacement in all subjects at 50% stance. This could be indicative of the thigh marker clusters not responding to the deceleration of the limb and thus continuing their forward motion relative to the shank. Knowledge of 3D motion in ACL deficient subjects is of interest for both understanding the injury mechanisms as well as the progression of degenerative joint disease. Recent studies have attempted to identify compensatory mechanisms in ACL deficient subjects using skin-marker based kinematics [20–22]. Although these studies associate altered tibio-femoral rotations and translations during gait [21,22] and a pivoting motion [20] with ACL deficiency, it is clear from the results of our investigation that the reported differences fall within the expected margin of error when predicting tibio-femoral kinematics using skin mounted markers. A set of standards for presentation of tibio-femoral kinematics seems needed and could be derived from the data in our study. Since the subjects had sterile bandages around the pin insertion sites and were instrumented with EMG electrodes, it is possible that the skin movement at or near these points could be reduced, similar to the findings of Manal et al. [1] when using so called under-wrap. The skin-markers were placed as far from the sterile bandages as possible, while still maintaining adequate marker separation. The EMG electrode placement over the vastus lateralis, vastus medialis and rectus femoris on the thigh and medial gastrocnemius on the shank is common in human movement analysis and
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therefore could represent a normal testing situation when combining EMG and motion analysis. Although as little wrapping as possible was used, it is possible that our testing setup did reduce skin movement in these areas. In addition, intra-cortical bone-pins could potentially alter the normal walking and hopping patterns of the subjects in this study. Previous studies have indicated that the kinematic profiles of subjects using this technique are similar to those using noninvasive techniques [4,6,9]. None of the subjects expressed discomfort while performing the walking or cutting trials in this study. With regards to the cutting trials, there is limited information to use for comparison however it is possible that the movement would be less vigorous when using bone-pins and possibly result in less skin movement. The results of this study could therefore be safely extended to others as, at the very least, a minimum approximation of skin movement during cutting and walking. The kinematics derived from the bone-pin-markers was used as a so called ‘gold standard’ in this study. This assumes the pins were rigidly fixed to the underlying bones and can be used to represent true bone motion. There are potential sources of error that could act alone or concurrently to contradict this assumption [4,9–11]: the pins could move in the bone, the marker cluster could move on the pin, the pin could bend and/or the pins could vibrate. Mechanical testing of the pins used in this study found that deflections larger than 0.4 mm caused permanent deformations that were visually detectable [11]. The orientation of the target clusters from the first reference trial was matched against the second to assess potential marker cluster movement or pin-bending. This, in addition to visual observation of removed pins for signs of pin bending, as well as in the RSA images when digitising, resulted in the exclusion of two subjects. The remaining six subjects showed no evidence of pin bending or marker cluster rotation and we therefore concluded that the pins were rigidly fixed to the bones and no bending or marker cluster movement corrupted the data. The bone-pin and marker-cluster complex resonant frequency was found to be 90 Hz [11] and was filtered out using the previously described low pass filter. We have therefore concluded that bone-pin derived kinematic measurement is a suitable ‘gold standard’ of measurement under our testing conditions. In this study, kinematic crosstalk was minimised by rotating the knee joint flexion axis to minimise abduction angle. This technique was tested on all six subjects however only two subjects showed moderately reduced abduction angles and were ‘corrected’ with this technique. This correction could potentially have masked true abduction/ adductions or internal/external rotations of the lower leg. However, it was decided that the reduction in artifact from kinematic crosstalk was of greater importance. RSA is highly accurate however the choice of the anatomical points is subject to human error [23]. Very small changes in digitised locations would amount to large changes in axial alignment of the anatomical coordinate system. The fact that four of six subjects required no axis realignment to reduce
kinematic crosstalk is an indication of well-chosen anatomical points and well-aligned anatomical coordinate systems. Furthermore, since the transformations and axes are equivalent for both the skin- and pin-markers, neither crosstalk nor the correction method would affect within subject comparisons. The determination of the anatomical reference points used to establish the anatomical coordinate systems proved to be far more difficult than originally anticipated. The anatomical differences across subjects were significant with respect to the medial and lateral edges of the tibia and femur, for example. This applies not only to the location of the point across subjects due to the size and location of the tibial eminence relative to the plateau or the depth of the intercondylar groove, but also the within subject relative position of one condyle to the other. This could explain intersubject differences in limb abduction/adduction angle, for example. In addition, if the knee joint was not fully extended during the RSA image collection then moving into a joint position more extended than this RSA image position will result in a hyperextension recorded during the moving trials. However, since the effective comparisons made in this study are within subject and made with the same reference systems within subject, the inter-subject differences in anatomical reference frame alignment will not affect the comparison of skin-marker to pin-marker kinematics. It should also be noted that standard skin-mounted anatomical reference markers were placed all subjects during the standard reference trials and were visible in the RSA images (medio-lateral femoral epicondyles and mediolateral tibial plateau). It was clear that the anatomical reference point skin-marker locations were not representative of the underlying anatomy. In spite of this they were relatively well-aligned to each other. Visual observation of the femoral condyles in the RSA images clearly shows anatomical alignment differences across subjects that would likely not be reflected when using skin-markers for anatomical reference frame alignment and could thus conceal natural limb position biases. The data from this study suggests that the use of skinmarkers to describe knee joint motion must be presented with an envelope of accuracy that describes the artifact imparted by skin movement of the markers. Although this error varies throughout the stance phases of gait and cutting, we propose the use of the average standard error of the estimate when reporting the accuracy of skin-marker derived kinematics. This estimate of the error (S) associated with predicting tibio-femoral kinematics from skin-markers would allow for the reporting of non-sagittal plane kinematics within approximately 65% confidence interval (for 95% confidence interval use 1.96 S) that may be relevant in situations where large differences between populations may be detected. Note that the use of S implies that the error is randomly distributed about the actual tibiofemoral kinematic parameter for a given measurement data point. The error in this study does not appear to be randomly
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distributed within each subject. However, the direction of the skin movement artifact is not repeatable across subjects in this study and others [1,4,6] where skin movement artifact has been evaluated. An error estimate that is not based on the direction of the error is therefore preferred.
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where n is the number of observations (comparisons), y the skin-marker derived kinematic data point, and x is the bonepin derived kinematic data point
References 5. Conclusions This study indicates that skin mounted reflective markers display significant limitations in predicting 3D kinematics of the knee joint. The absolute errors presented in this study offer a guideline to which conclusions may be drawn from 3D knee joint kinematics for walking and cutting motions. Although surface marker attachment methods affect knee joint kinematics these affects are below those caused by skin movement artifacts as reported in this study. We therefore propose the use of a standard error of measurement when presenting knee joint kinematic data. The data presented in Table 3 could be used as guidelines when discussing findings across populations. An additional finding of this study is that the surface marker derived kinematics can present repeatable profiles within a subject for various movements (Figs. 4 and 5). These repeatable patterns must not be misinterpreted as accurately representing skeletal kinematics, at least beyond the sagittal plane of movement where the error is small relative to the total movement. When measuring knee joint kinematics under similar conditions observations based on measurements below the standard errors described in this study must be guarded.
Acknowledgements The authors would like to thank Birgitta Runtze for her aid with the RSA data and Mark Carpenter for his advice with data analysis and the manuscript in general. This project was partially funded by grants from the Centrum for Idrottsforskning-Sweden and Nature Sciences and Engineering Research Council-Canada.
Appendix A Standard error of the estimate: a measure of the error associated with predicting the value of x from the dependant observation y: sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi X 2ffi X 1 S¼ y n y2 nðn 2Þ 2 P P P n xy x y 2 P P n x2 x
[1] Manal K, McClay I, Stanhope S, Richards J, Galinat B. Comparison of surface mounted markers and attachment methods in estimating tibial rotations during walking: an in vivo study. Gait Posture 2000;11:38– 45. [2] Cappozzo A, Catani F, Leardini A, Benedetti MG, Croce UD. Position and orientation in space of bones during movement: experimental artifacts. Clin Biomech 1996;11:90–100. [3] Leardini A, Chiari L, Della CU, Cappozzo A. Human movement analysis using stereophotogrammetry. Part 3. Soft tissue artifact assessment and compensation. Gait Posture 2004. [4] Reinschmidt C, van den Bogert AJ, Nigg BM, Lundberg A, Murphy N. Effect of skin movement on the analysis of skeletal knee joint motion during running. J Biomech 1997;30:729–32. [5] Ramsey DK, Lamontagne M, Wretenberg PF, Valentin A, Engstrom B, Nemeth G. Assessment of functional knee bracing: an in vivo threedimensional kinematic analysis of the anterior cruciate deficient knee. Clin Biomech 2001;16:61–70. [6] Houck J, Yack HJ, Cuddeford T. Validity and comparisons of tibiofemoral orientations and displacement using a femoral tracking device during early to mid stance of walking. Gait Posture 2004; 19:76–84. [7] Tashman S, Collon D, Anderson K, Kolowich P, Anderst W. Abnormal rotational knee motion during running after anterior cruciate ligament reconstruction. Am J Sport Med 2004;32:975–83. [8] Ramsey DK, Wretenberg PF. Biomechanics of the knee: methodological considerations in the in vivo kinematic analysis of the tibio-femoral and patellofemoral joint. Clin Biomech 1999;14:595– 611. [9] Lafortune MA, Cavanagh PR, Sommer III HJ, Kalenak A. Threedimensional kinematics of the human knee during walking. J Biomech 1992;25:347–57. [10] Lundberg A. On the use of bone and skin-markers for human movement research. Hum Movement Sci 1996;15:411–22. [11] Ramsey DK, Wretenberg PF, Benoit DL, Lamontagne M, Nemeth G. Methodological concerns using intra-cortical pins to measure tibiofemoral kinematics. Knee Surg Sport Tr A 2003;11:344–9. [12] Levens AS, Inmanm VT, Blosser JA. Transverse rotation of the segments of the lower extremity in locomotion. J Bone Joint Surg (Am) 1948;30:859–72. [13] Lafortune MA. Three-dimensional acceleration of the tibia during walking and running. J Biomech 1991;24:877–86. [14] Von Porat A, Roos EM, Roos H. High prevalence of osteoarthritis 14 years after an anterior cruciate ligament tear in male soccer players: a study of radiographic and patient relevant outcomes. Br J Sport Med 2004;38:263. [15] Peterson L, Renstrom PA. Sports injuries: their prevention and treatment, 3rd ed., Martin Duntz; 2003. p. 271–93. [16] Lafontaine D, Benoit DL, Lamontagne M, Xu L. Validation of joint rotation and translation calculations using a joint coordinate system approach. In: Proceedings of the 12th annual meeting of the European society of movement analysis for adults and children; 2003. [17] Grood ES, Suntay WJ. A joint coordinate system for the clinical description of three-dimensional motions: application to the knee. J Biomech Eng 1983;105:136–44. [18] Challis JH. A procedure for determining rigid body transformation parameters. J Biomech 1995;28:733–7. [19] Manal K, McClay DI, Galinat B, Stanhope S. The accuracy of estimating proximal tibial translation during natural cadence walking: bone vs. skin mounted targets. Clin Biomech 2003;18:126–31.
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[20] Ristanis S, Giakas G, Papageorgiou CD, Moraiti T, Stergiou N, Georgoulis AD. The effects of anterior cruciate ligament reconstruction on tibial rotation during pivoting after descending stairs. Knee Surg Sport Tr A 2003;11:360–5. [21] Knoll Z, Kocsis L, Kiss RM. Gait patterns before and after anterior cruciate ligament reconstruction. Knee Surg Sport Tr A 2004;12:7–14.
[22] Georgoulis AD, Papadonikolakis A, Papageorgiou CD, Mitsou A, Stergiou N. Three-dimensional tibio-femoral kinematics of the anterior cruciate ligament-deficient and reconstructed knee during walking. Am J Sport Med 2003;31:75–9. [23] Ryd L, Yuan X, Lofgren H. Methods for determining the accuracy of radiostereometric analysis (RSA). Acta Orthop Scand 2000;71:403–8.
Effect of skin movement artifact on knee kinematics during gait and cutting motions measured in vivo Daniel L. Benoit a,b,c,*, Dan K. Ramsey d, Mario Lamontagne f,g, Lanyi Xu f, Per Wretenberg b,e, Per Renstro¨m a,b a
Institution for Surgical Sciences, Section of Sports Medicine, Karolinska Institute, Stockholm, Sweden b Department of Orthopaedics, Karolinska Hospital, Stockholm, Sweden c Department of Mechanical Engineering, University of Delaware, 106 Spencer Lab, Newark, DE 19711, USA d Department of Physical Therapy, University of Delaware, Newark, DE, USA e Institution for Surgical Sciences, Section of Orthopaedics, Karolinska Institute, Stockholm, Sweden f School of Human Kinetics, University of Ottawa, Ottawa, Canada g Department of Mechanical Engineering, University of Ottawa, Ottawa, Canada Received 6 November 2004; received in revised form 25 March 2005; accepted 9 April 2005
Abstract Eight healthy male subjects had intra-cortical bone-pins inserted into the proximal tibia and distal femur. Three reflective markers were attached to each bone-pin and four reflective markers were mounted on the skin of the tibia and thigh, respectively. Roentgenstereophotogrammetric analysis (RSA) was used to determine the anatomical reference frame of the tibia and femur. Knee joint motion was recorded during walking and cutting using infrared cameras sampling at 120 Hz. The kinematics derived from the bone-pin markers were compared with that of the skin-markers. Average rotational errors of up to 4.48 and 13.18 and translational errors of up to 13.0 and 16.1 mm were noted for the walk and cut, respectively. Although skin-marker derived kinematics could provide repeatable results this was not representative of the motion of the underlying bones. A standard error of measurement is proposed for the reporting of 3D knee joint kinematics. # 2005 Elsevier B.V. All rights reserved. Keywords: Soft tissue artifacts; Movement analysis; In vivo; Three-dimensional analysis; Knee joint
1. Introduction One of the most common methods to measure knee joint motion is to track the motion of clusters of three or more retro-reflective or light emitting markers affixed to the skin of the shank and thigh. The marker configurations used may influence the accuracy of the reconstructed data [1]. However, other factors may play a more significant role in determining the validity of the results. When applied to measuring knee joint kinematics based on the position of the tibia and femur, the accuracy of these measurements is prone * Corresponding author at: Department of Mechanical Engineering, University of Delaware, Spencer Labs 126, Newark, DE 19716, USA. Tel.: +1 302 831 2410/2423; fax: +1 302 831 3466/3619. E-mail address: [email protected] (D.L. Benoit). 0966-6362/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2005.04.012
to error due to skin movement artifact [2]. A recent review by Leardini et al. [3] identifies that previous investigations have been lacking in sample size [4], or have had methodological limitations [5,6]. While only three and two subjects were evaluated in these studies, respectively, the lack of agreement between the shape of the kinematic profiles derived from the skin- and pin-markers poses an important question as to how well skin-marker kinematic profiles represent the underlying bones. Others have used different techniques to quantify movement artifact on the shank and thigh [2] but the subjects investigated were from a population recovering from leg fractures. In addition, only two subjects were available with thigh mounted pin-markers and no subjects were simultaneously instrumented with pin-markers on both the shank and thigh. Recent progress using a 250 frame/s
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stereoradiographic system is encouraging [7] but the confined area of measurement limits the movement possibilities of the subject. Ideally, kinematic data would be reported with a standard error of measurement that reflects the uncertainty of the reported findings caused by this skin movement artifact inherent in the measurement technique. When comparing two groups of subjects and attempting to detect kinematic differences associated with a population difference the findings could be confidently reported with the knowledge that observed differences are due to the population differences and not measurement error. Tracking the motion of the tibia and femur with surgically implanted intra-cortical bone-pins instrumented with clusters of markers is an accurate means of directly measuring skeletal motion under physiologically relevant testing conditions [8]. Target clusters are tracked using any one of the commercially available motion analysis systems and movement of the underlying bones can be derived. The use of percutaneous bone-pins mounted in the tibia and femur and instrumented with no less than three reflective markers can provide rigid body reconstruction using motion analysis. Roentgen-stereophotogrammetric analysis (RSA) has been used to relate the position of these markers to the anatomical reference frame and to derive an anatomical coordinate system to describe motion [9]. The principal is to reconstruct the position of the bone-embedded markers to an anatomical reference point, such as the deepest point of the intercondylar groove for the femur and the most proximal point of the medial condylar eminence for the tibia [4,5]. The anatomical reference points are used to determine the origin of each segment, respectively. Using RSA it is possible to apply a bone-embedded, or anatomical, reference system when describing joint motion in a laboratory reference frame. This simplifies data interpretation and, given an accurate and reproducible choice of anatomical reference points and coordinate system alignment, allows comparisons not only within subjects but also potentially across subjects. Combining RSA with bone-pins allows an accurate representation of the bones but is technically difficult and invasive [10,11]. However, the advantages include the ability to accurately represent tibio-femoral kinematics and, although an invasive technique, subjects have been shown to walk [5,6,9,12], run [4,9,13] and hop [5] normally. Knowledge of non-sagittal plane tibio-femoral kinematics is necessary if we are to improve our knowledge of the mechanisms associated with knee joint injury and the progression of knee joint degeneration. For example, the anterior cruciate ligament (ACL) injury is believed to lead to degenerative joint disease [14]. Since injury mechanisms of the ACL are thought to combine tibio-femoral rotation with anterior tibial translation [15], knowledge of combined sagittal and non-sagittal plane tibio-femoral joint motion under physiological conditions is essential for detecting critical phases of motion that may predispose the ACL to
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loading. To our knowledge there is no information in the literature about the ability to accurately measure tibiofemoral joint motion in non-sagittal plane movements. This lack of information seriously limits the ability to investigate knee joint injury mechanisms using non-invasive techniques. The purpose of this investigation is to quantify the error caused by skin movement artifact when reporting the kinematics of the tibio-femoral joint during movements that incorporate sagittal and non-sagittal plane rotations. We hypothesise that skin movement error will reduce the ability to accurately measure 3D tibio-femoral kinematics and that non-sagittal plane movements will be most affected by skin movement artifact.
2. Methods 2.1. Subjects Eight healthy, moderately active, male subjects with no history of knee injury or prior surgical treatment of the lower limbs were studied (Table 1). Informed consent was obtained from the subjects and the study was approved by the Ethics Committee of the Karolinska Hospital, Stockholm, Sweden. 2.2. Surgical procedure Stainless steel Apex self-drilling/self-tapping pins (Stryker Howmedica AB Sweden, 3.0 mm diameter, #5038-2110) were inserted under local anaesthetic into the distal femur and proximal tibia of the right leg [11] at the Karolinska University Hospital (Stockholm, Sweden). The femoral pin was inserted between the Iliotibial (IT) band and the quadriceps tendon superior of the vastus lateralis to minimise impingement problems. Following surgery subjects performed active flexion and extension movements while standing to identify whether movement restrictions were evident. Subjects were then transported by wheelchair to the motion analysis laboratory for data collection. The pins remained inserted for the duration of the test. Upon
Table 1 Subject characteristics Subject
Age
Height (cm)
Weight (kg)
1 2 3 4 5 6 7 8
32 22 22 32 31 27 22 22
185 181 180 171 174 178 181 175
89 78 78 86 62 76 93 63
Average
26
178.1
78.1
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completion of the experiments (approximately 2 h), subjects returned to the operating theatre to have the dressing and pins removed. 2.3. Motion recordings
Fig. 1. (a) Picture of the bone-pin and surface marker configurations for a representative subject. Note: the pins are inserted in the tibia and femur, respectively. Each pin is instrumented with a target cluster, comprised of four reflective markers. The skin is instrumented with four reflective surface markers; (b) RSA procedure and calibration box. The right leg is extended
Triads of three non-collinear 7 mm reflective markers (pin-markers) were affixed to the pins. Additional clusters of four 10 mm surface markers (skin-markers) were affixed onto the lateral and frontal aspects of both the right thigh and shank (Fig. 1a and b). Skin-markers were spaced 10–15 cm from adjacent markers within their respective cluster and their arrangement was chosen to ensure they remained noncoplanar in at least two camera views throughout the range of motion. Reflective markers were also placed on the right heel, 5th metatarsal and lateral malleolus. Bone-pin and skin-marker trajectories were tracked within 0.8 m3 measurement volume (1.1 m 0.8 m 0.9 m) using four infrared cameras (ProReflex, Qualisys AB, Sweden), sampling at 120 Hz. Marker coordinates were transformed using the direct linear transform (DLT) and the raw 3D coordinates exported and saved to a local computer for analysis. The motion analysis system simultaneously collected both the skin- and pin-marker configurations for each standing and movement trial. Participants were asked to perform a series of normal walking trials and lateral cutting manoeuvres. Each subject was given several practice trials to familiarise themselves with the pins and testing protocol. Ground reaction forces (GRF) were measured simultaneously at 960 Hz using a Kistler force plate (Kistler Instruments AG, Winterhur, Switzerland) located midway through the measurement volume. For gait testing, subjects walked along a 12 m walkway at a selfselected pace. Contact with the force plate and no evidence of targeting were required for a trial to be considered. Before performing the lateral cutting manoeuvre, subjects jumped for maximal horizontal distance. Their longest measurement was recorded and marked on the floor to determine the proper takeoff distance to the force platform. From an initial standing position the subject pushed off using the left leg and, upon landing onto their right foot, immediately pushed off the platform, cutting to the left at an angle of approximately 458. Five measurement trials were recorded for each movement task as well as a standing reference trial before and after each block of movement trials. Subjects stood in a neutral position and were instructed to align their feet parallel to the force platform to define the tibial and femoral anatomical coordinate systems. The orientation of the target clusters from the first reference trial was matched against the second to verify the pins did not bend and the triad did not rotate during testing. through the box with the bone-pins and reflective markers in place. The knee is flexed between 08 and 108, RSA recordings were taken following motion analysis sessions.
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2.4. RSA technique and anatomical reference frame Following the motion analysis recordings, the leg was extended through a biplanar calibration box (Cage 10, RSA Biomedical Innovations, Umea˚, Sweden) and biplanar radiographs (RSA) were recorded (Fig. 1b). All radiographs were taken with the subject supine and the knee flexed between 08 and 108. From these radiographs, two local anatomical reference points were identified and digitised with the aid of an experienced RSA technician (Sahlgrenska University Hospital Gothenburg, Sweden; see acknowledgements). In total, 19 points were digitised to derive the anatomical reference system using UMRSA software (version 5, Biomedical Innovations-AB, Umea, Sweden). These included: 1–4. 5. 6. 7–8. 9.
10–14. 15.
16. 17–18. 19.
Tibial pin-markers. Proximal medial tibial eminence (tibial reference point). The most distal point along a line trough point 5 and parallel to the long axis of the tibia. Medial and lateral edges of proximal tibia respectfully. A distal point along a line drawn perpendicular to the long axis of the tibia and running originating at the tibial reference point. Femoral pin-markers. Proximal (deepest) point of the condylar groove (notch) (femoral reference point). The most distal point along a line trough point 15 and parallel to the long axis of the femur. Medial and lateral edges of the distal femur, respectively. A distal point along a line drawn perpendicular to the long axis of the femur and originating at the femoral reference point.
Zt
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vector joining points 5 and 6; from the tibial origin directed longitudinally along the tibial axis in the frontal plane.
2.5. Kinematic technique Custom written software (Matlab, Mathworks, USA) was developed and validated to process the 3D kinematic information derived from the bone-pins and surface markers, respectively [16]. The kinematic profile was described using the terminology and the ordered sequence of the Joint Coordinate System (JCS) [17]. In brief, the bone-embedded coordinate system is defined from the RSA coordinate data: the digitised points are used to locate the origin and direction of the anatomical reference frames. Transformation matrices for the pin-markers of both tibia and femur were derived to relate the position of these points to their respective anatomical origins [17,18]. 3D pin-marker coordinates from the standing reference trials (SRT) were used to determine the transformation matrix from the laboratory reference frame to the bone-embedded reference frame. This transformation matrix was then used to determine the location of the skin-markers with respect to the boneembedded reference frame (Fig. 2). Kinematic data for both the pin- and skin-markers were derived and low-passed filtered at 12 Hz using a 20th order FIR digital filter (Matlab). The cut-off frequency was determined by running a Fourier analysis that retained 95% of the original signal (both angular and linear data) and by visual inspection. The limited measurement volume allowed recording of a limited pre-foot-strike phase and complete stance phase of the walking and cutting movements. Foot-strike and toe-off were determined using the force platform data and the corresponding frame number was identified in the kinematic data. The kinematic data was normalised to 100% stance
The origin of the femoral reference frame was located at the deepest point of the intercondylar groove (point 15). The origin of the tibial reference frame was located at the highest point of the medial intercondylar eminence (point 5). Local coordinate systems of the femur and tibia were defined as follows: Xf Yf Zf
Xt Yt
cross product of vectors Zf and Yf; from the femoral origin, directed laterally. cross product of Zf and vector joining points 17 and 18; from the femoral origin, directed anteriorly. vector joining points 15 and 16; from the femoral origin directed longitudinally along the femoral axis in the frontal plane. cross product of vectors Zt and Yt; from the tibial origin, directed laterally. cross product of Zt and vector joining points 7 and 8; from the tibial origin, directed anteriorly.
Fig. 2. Schematic representation of the anatomical reference frames and the bone-pin marker cluster configurations. Adapted from Benoit DL (2005): motion analysis of the knee: kinematic artifacts, EMG normalisation and joint forces. Ph.D. thesis, Karolinska Institutet, Stockholm.
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phase (foot-strike to toe-off = 100%). Pre-foot-strike was expressed as a function of the normalised stance phase and ranges from 10% (or the longest duration of pre-foot-strike for that given subject) to 0% (foot-strike). 2.6. Statistical analysis Three points of interest during the stance phase of the walking and cutting cycle were chosen for statistical analysis: heel strike (HS); mid-stance point (corresponding with maximum knee flexion angle during the first 60% of stance) (MS); and toe-off (TO). The kinematic data derived from the bone-pins was considered the ‘gold standard’ of measurement. Paired, two-tailed Student’s ttests were used to determine if skin derived kinematics at the three time-points differed from those derived from the bone-pins. Kinematic data at HS, MS, TO are often extracted and used for comparisons of populations in gait studies. As we were interested in the validity of making such comparisons, we chose to treat each extracted point as independent. Accuracy of the skin-marker kinematics was calculated as the absolute difference between skin and pin knee flexion/extension, abduction/adduction and internal/external rotation angles and medio/lateral, antero/posterior and distraction/compression translations at HS, MS and TO. In addition, the standard error of estimate (S) was calculated for both walking and cutting. In this approach, the error is implicitly assumed to arise entirely from the skinmarker data (Y), while the pin-marker data (X) is assumed to be without error (E). In other words, since we assume that X for a given point in time is accurate, then Y will predict X such as (Y + E) within a certain confidence interval for that given time point (see Appendix A for a description of S). This data was calculated by comparing the pin- and skinmarker data across all subjects for each trial and at every time point, with the average calculated across time points (total number of time points: n = 110 walking, n = 105 cutting due to a shorter observed pre-foot-strike phase in some subjects).
3. Results Of the eight subjects, two subjects (numbers one and three in Table 1) had data that were not usable: one subject was excluded due to incomplete RSA data that rendered transformation impossible, while the second subject bent the femoral pin during knee flexion, the result of an interaction with the soft tissue and musculature. No subjects experienced significant pain and/or discomfort during the experiments and all reported being able to move their knee freely despite pin implantation. However, one subject was limited to three trials for both walking and cutting while another was limited to three trials for walking as recommended by the attending surgeon to reduce exposure time for these subjects. Simultaneously recorded high-speed digital video files (100 frames/s; JVC model DVL9000, Japan) of the motions indicated that all subjects contacted the force plate with the heel during walking and the mid-foot during cutting. Figs. 3 and 4 display rotations and translations of a representative subject during both walking and cutting, respectively. Absolute error between the skin-marker and pin-marker kinematics at heel strike, mid-stance and toe-off during the walking and cutting motions are noted in Table 2. A significant difference in reporting skin-marker derived kinematics with respect to actual tibio-femoral kinematics is evidenced at heel strike, mid-stance and toe-off for both walking and cutting rotations and translations. In the stance phase of walking the average rotational absolute error ranged from 2.48 to 4.48 while translational errors ranged from 3.3 to 13.0 mm. In the cutting movement the range of absolute errors and maximum absolute error were higher for both rotations (3.38 to 13.18) and translations (5.6 to 16.1 mm) respectively. The relationship between skin and pin derived kinematic profiles observed across subjects differed considerably. Figs. 5 and 6 illustrate the average error due to skin movement for each during the stance phase of walking and cutting, respectively. In Figs. 5 and 6 a positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-
Table 2 Absolute error values of skin-marker derived kinematics at three time points during walking and cutting of knee rotations and translations: flexion–extension (Flex/Ext), adduction–abduction (Add/Abd), internal–external rotation (Int/Ext); medio–lateral (Med/Lat), anterior–posterior (Ant/Post) and distraction– compression (Dist/Comp) Rotations (degrees S.D.) Flex/Ext
Add/Abd
Translations (mm S.D.) Int/Ext
Med/Lat
Ant/Post
Dist/Comp
Walk Foot-strike Mid-stance Toe-off
2.8 (2.6)a 2.4 (2.0)a 2.7 (2.4)
2.5 (2.7) 3.1 (3.3) 4.4 (3.2)a
2.8 (2.0)a 2.4 (1.1) 2.2 (2.1)
5.0 (2.6) 5.5 (3.1)a 8.0 (5.7)
7.7 (4.4)a 6.2 (5.4) 13.0(5.0)a
5.0 (2.9)a 3.3 (2.4)a 5.0 (2.5)a
Cut Foot-strike Mid-stance Toe-off
3.9 (2.9) 4.0 (2.5) 4.2 (2.7)
6.7 (5.4)a 5.9 (3.1)a 13.1 (9.8)
5.4 (4.2)a 5.4 (4.0)a 3.3 (1.8)a
7.3 (4.4) 5.9 (4.5)a 13.9(10.1)
5.6 (5.1)a 6.7 (4.4)a 16.1 (8.9)
6.3 (4.0)a 5.6 (3.8)a 8.3 (6.2)a
a
Significant difference between skin- and pin-marker data (two-tailed paired Student’s t-test, p < 0.05).
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Fig. 3. Walking trials of a representative subject, subject-4. Knee joint flexion (+)/extension () (Flex/Ext), adduction (+)/abduction () (Add/Abd) and internal (+)/external () (Int/Ext) rotation data is presented in the left column while lateral (+)/medial () (Med/Lat), anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp) are in the right column. Pin-marker labels are unfilled, skin-markers in bold.
marker derived knee joint rotations and translations. During walking (Fig. 5) there appears to be some agreement across subjects in the shape of the error profile for some rotations (flexion/extension; internal/external) and translations (anterior/posterior; distraction/compression). With respect to the
magnitude and direction of the error (over or under-estimation of joint position) there appears to be some agreement for distraction/compression. During cutting (Fig. 6) there appears to be greater agreement in the shape of the error curves for both rotations
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Fig. 4. Cut movement trials of a representative subject, subject-4. Knee joint flexion (+)/extension () (Flex/Ext), adduction (+)/abduction () (Add/Abd) and internal (+)/external () (Int/Ext) rotation data is presented in the left column while lateral (+)/medial () (Med/Lat), anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp) are in the right column. Pin-marker labels are unfilled, skin-markers in bold.
(adduction/abduction, internal/external rotation) and translations (lateral/medial; antero/posterior) while the magnitude and direction of the error (over or under-estimation of joint position) also shows agreement for distraction/ compression and antero/posterior translations. While the absolute error is the absolute difference between the skin-marker and pin-marker derived kinematics, the average standard error of the estimate (S)
describes the error associated with predicting pin-marker based tibio-femoral kinematics from skin-marker derived kinematics. The average S for walking and cutting movements is found in Table 3 and represents the expected margin of error when predicting tibio-femoral joint motion using skin-markers. These error values were higher in the cutting movement for both rotations and translations.
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Fig. 5. Progression of error due to skin movement during walking for all subjects. Figure show the average difference between skin-marker and pin-marker data for each subject as it progressive during stance. A positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-marker derived knee joint rotations and translations. Left column: knee joint flexion (+)/extension () (Flex/Ext); adduction (+)/ abduction () (Add/Abd) and internal (+)/external () (Int/Ext). Right column: lateral (+)/medial () (Med/Lat); anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp).
4. Discussion The purpose of this investigation was to quantify the error caused by skin movement artifact when reporting the kinematics of the tibio-femoral joint during movements that
incorporate sagittal and non-sagittal plane rotations. Skin movement artifact is inherent in motion analysis using surface markers and this study represents a comprehensive record of the effect of skin movement during gait in healthy subjects and, to our knowledge, the only record of the effect
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Fig. 6. Progression of error due to skin movement during cutting for all subjects. It shows the average difference between skin-marker and pin-marker data for each subject as it progressive during stance. A positive value describes an over-estimation, zero described perfect agreement and negative values describe an under-estimation of the skin-marker derived knee joint rotations and translations. Left column: knee joint flexion (+)/extension () (Flex/Ext); adduction (+)/ abduction () (Add/Abd); internal (+)/external () (Int/Ext). Right column: lateral (+)/medial ()() (Med/Lat); anterior (+)/posterior () (Ant/Post) and distraction (+)/compression () (Dist/Comp).
of skin movement during the cutting movement. We found within subject data to be repeatable when using either the skin or pin mounted markers for both the walk and cut. This was encouraging however as the error associated with skin movement artifact differed widely across subjects. Skin movement of the thigh and shank may be large enough to
mask the actual movements of the underlying bones, thus making reporting of knee joint kinematics using skinmarkers potentially uncertain. With three subjects Reinschmidt et al. [4] reported average errors relative to the range of motion of the knee during the stance phase of running of 21% (flexion/
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Table 3 Average standard error of the estimate (S) describing the error associated with predicting tibio-femoral kinematics from skin-marker derived kinematics Rotations (8)
Walk Cut
Translations (mm)
Flex/Ext
Add/Abd
Int/Ext
Med/Lat
Ant/Post
Dist/Comp
2.5 6.3
3.6 4.5
2.9 3.0
5.9 8.0
6.8 5.5
2.7 7.1
Average calculated for each data point of the stance phase (average of 110 data points) based on the estimated prediction of all walking (n = 25) and cutting (n = 28) trials. For a description of S see Appendix A.
extension), 63% (internal/external rotation) and 70% (abduction/adduction). No discussion of the error in recording joint translation was reported while an inadequate calibration area added 28 measurement error to the rotational data. Though only two subjects were observed over a limited stance time, Houck et al. [6] found absolute differences of up to 2.28 in the sagittal plane, 2.78 in the frontal plane and 1.88 in the transverse plane, while up to 13.9 mm of linear displacement was observed during walking. The results of these studies are comparable to those observed in our study. Comparing kinematic data collected simultaneously from surface markers and that of bone-embedded marker systems fixed to an external fixation device, Cappozzo et al. [2] reported skin-marker movement of 1–3 cm on the shank and thigh, respectively leading to slightly higher rotational errors then found in our study. However, the external fixator and the fracture suffered by the subjects may have affected the normal skin movement, walking ability and normal muscle mass of the test subjects. Using an externally fixed ‘bone tracker’ Manal et al. [1,19] found that linear translations of the knee joint using skin-markers of 2.1–7 mm depending on the plane of movement, with average rotation errors below 38. Individual subject deviations ranged between 48 and 78, depending on the skin-marker configuration. These observations were solely related to skin movement of the shank during the stance phase of walking. It can be reasoned that errors would likely have been higher had the effect of thigh skin movement also been measured however the fact that their results are comparable to our study shows promise for the use of less invasive techniques to track bone motion. With respect to walking, the profile of the error curves appears to be somewhat similar in flexion/extension, internal/ external rotation, anterior/posterior translation and distraction/compression. However, the direction of the error (over/ under-estimation) differs widely in magnitude. It seems that if the initial error could be estimated at a given time point (footstrike for example), the error could potentially be predicted for that subject and the aforementioned parameters. This however requires further investigation. The error of subject 5 during walking consistently differs from that of the other subjects around 60% of the stance phase. Using the marker tracking portion of the QTrac (Qualisys AB, Sweden) analysis software, visual inspection of this subject’s raw pin-marker data revealed that tibiofemoral motion did occur around this time point when visualised with the pin-markers. This movement pattern was
not witnessed using the skin-markers and thus contributed to the altered error pattern around this time point. We believe that the skin-markers were incapable of tracking this underlying motion, as it should have been simultaneously detected. The bone-pins and marker triad of this subject were not found to be damaged or loosened upon removal and this occurrence was not witnessed during the cutting trial, which was performed after the walking trials. We therefore believe this detected motion was a function of their walking style and anatomy. During the cut the profile of the error curves appears to be more consistent than during walking. While the error magnitudes are generally larger it appears that the skin moves in a more consistent pattern across subjects and indicates that the skin-markers were not sensitive enough to track the motions of the underlying bones for this more ballistic movement. The most important example is in the measure of anterior/posterior tibial translation where skinmarker kinematics would have indicated a posterior displacement in all subjects at 50% stance. This could be indicative of the thigh marker clusters not responding to the deceleration of the limb and thus continuing their forward motion relative to the shank. Knowledge of 3D motion in ACL deficient subjects is of interest for both understanding the injury mechanisms as well as the progression of degenerative joint disease. Recent studies have attempted to identify compensatory mechanisms in ACL deficient subjects using skin-marker based kinematics [20–22]. Although these studies associate altered tibio-femoral rotations and translations during gait [21,22] and a pivoting motion [20] with ACL deficiency, it is clear from the results of our investigation that the reported differences fall within the expected margin of error when predicting tibio-femoral kinematics using skin mounted markers. A set of standards for presentation of tibio-femoral kinematics seems needed and could be derived from the data in our study. Since the subjects had sterile bandages around the pin insertion sites and were instrumented with EMG electrodes, it is possible that the skin movement at or near these points could be reduced, similar to the findings of Manal et al. [1] when using so called under-wrap. The skin-markers were placed as far from the sterile bandages as possible, while still maintaining adequate marker separation. The EMG electrode placement over the vastus lateralis, vastus medialis and rectus femoris on the thigh and medial gastrocnemius on the shank is common in human movement analysis and
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therefore could represent a normal testing situation when combining EMG and motion analysis. Although as little wrapping as possible was used, it is possible that our testing setup did reduce skin movement in these areas. In addition, intra-cortical bone-pins could potentially alter the normal walking and hopping patterns of the subjects in this study. Previous studies have indicated that the kinematic profiles of subjects using this technique are similar to those using noninvasive techniques [4,6,9]. None of the subjects expressed discomfort while performing the walking or cutting trials in this study. With regards to the cutting trials, there is limited information to use for comparison however it is possible that the movement would be less vigorous when using bone-pins and possibly result in less skin movement. The results of this study could therefore be safely extended to others as, at the very least, a minimum approximation of skin movement during cutting and walking. The kinematics derived from the bone-pin-markers was used as a so called ‘gold standard’ in this study. This assumes the pins were rigidly fixed to the underlying bones and can be used to represent true bone motion. There are potential sources of error that could act alone or concurrently to contradict this assumption [4,9–11]: the pins could move in the bone, the marker cluster could move on the pin, the pin could bend and/or the pins could vibrate. Mechanical testing of the pins used in this study found that deflections larger than 0.4 mm caused permanent deformations that were visually detectable [11]. The orientation of the target clusters from the first reference trial was matched against the second to assess potential marker cluster movement or pin-bending. This, in addition to visual observation of removed pins for signs of pin bending, as well as in the RSA images when digitising, resulted in the exclusion of two subjects. The remaining six subjects showed no evidence of pin bending or marker cluster rotation and we therefore concluded that the pins were rigidly fixed to the bones and no bending or marker cluster movement corrupted the data. The bone-pin and marker-cluster complex resonant frequency was found to be 90 Hz [11] and was filtered out using the previously described low pass filter. We have therefore concluded that bone-pin derived kinematic measurement is a suitable ‘gold standard’ of measurement under our testing conditions. In this study, kinematic crosstalk was minimised by rotating the knee joint flexion axis to minimise abduction angle. This technique was tested on all six subjects however only two subjects showed moderately reduced abduction angles and were ‘corrected’ with this technique. This correction could potentially have masked true abduction/ adductions or internal/external rotations of the lower leg. However, it was decided that the reduction in artifact from kinematic crosstalk was of greater importance. RSA is highly accurate however the choice of the anatomical points is subject to human error [23]. Very small changes in digitised locations would amount to large changes in axial alignment of the anatomical coordinate system. The fact that four of six subjects required no axis realignment to reduce
kinematic crosstalk is an indication of well-chosen anatomical points and well-aligned anatomical coordinate systems. Furthermore, since the transformations and axes are equivalent for both the skin- and pin-markers, neither crosstalk nor the correction method would affect within subject comparisons. The determination of the anatomical reference points used to establish the anatomical coordinate systems proved to be far more difficult than originally anticipated. The anatomical differences across subjects were significant with respect to the medial and lateral edges of the tibia and femur, for example. This applies not only to the location of the point across subjects due to the size and location of the tibial eminence relative to the plateau or the depth of the intercondylar groove, but also the within subject relative position of one condyle to the other. This could explain intersubject differences in limb abduction/adduction angle, for example. In addition, if the knee joint was not fully extended during the RSA image collection then moving into a joint position more extended than this RSA image position will result in a hyperextension recorded during the moving trials. However, since the effective comparisons made in this study are within subject and made with the same reference systems within subject, the inter-subject differences in anatomical reference frame alignment will not affect the comparison of skin-marker to pin-marker kinematics. It should also be noted that standard skin-mounted anatomical reference markers were placed all subjects during the standard reference trials and were visible in the RSA images (medio-lateral femoral epicondyles and mediolateral tibial plateau). It was clear that the anatomical reference point skin-marker locations were not representative of the underlying anatomy. In spite of this they were relatively well-aligned to each other. Visual observation of the femoral condyles in the RSA images clearly shows anatomical alignment differences across subjects that would likely not be reflected when using skin-markers for anatomical reference frame alignment and could thus conceal natural limb position biases. The data from this study suggests that the use of skinmarkers to describe knee joint motion must be presented with an envelope of accuracy that describes the artifact imparted by skin movement of the markers. Although this error varies throughout the stance phases of gait and cutting, we propose the use of the average standard error of the estimate when reporting the accuracy of skin-marker derived kinematics. This estimate of the error (S) associated with predicting tibio-femoral kinematics from skin-markers would allow for the reporting of non-sagittal plane kinematics within approximately 65% confidence interval (for 95% confidence interval use 1.96 S) that may be relevant in situations where large differences between populations may be detected. Note that the use of S implies that the error is randomly distributed about the actual tibiofemoral kinematic parameter for a given measurement data point. The error in this study does not appear to be randomly
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distributed within each subject. However, the direction of the skin movement artifact is not repeatable across subjects in this study and others [1,4,6] where skin movement artifact has been evaluated. An error estimate that is not based on the direction of the error is therefore preferred.
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where n is the number of observations (comparisons), y the skin-marker derived kinematic data point, and x is the bonepin derived kinematic data point
References 5. Conclusions This study indicates that skin mounted reflective markers display significant limitations in predicting 3D kinematics of the knee joint. The absolute errors presented in this study offer a guideline to which conclusions may be drawn from 3D knee joint kinematics for walking and cutting motions. Although surface marker attachment methods affect knee joint kinematics these affects are below those caused by skin movement artifacts as reported in this study. We therefore propose the use of a standard error of measurement when presenting knee joint kinematic data. The data presented in Table 3 could be used as guidelines when discussing findings across populations. An additional finding of this study is that the surface marker derived kinematics can present repeatable profiles within a subject for various movements (Figs. 4 and 5). These repeatable patterns must not be misinterpreted as accurately representing skeletal kinematics, at least beyond the sagittal plane of movement where the error is small relative to the total movement. When measuring knee joint kinematics under similar conditions observations based on measurements below the standard errors described in this study must be guarded.
Acknowledgements The authors would like to thank Birgitta Runtze for her aid with the RSA data and Mark Carpenter for his advice with data analysis and the manuscript in general. This project was partially funded by grants from the Centrum for Idrottsforskning-Sweden and Nature Sciences and Engineering Research Council-Canada.
Appendix A Standard error of the estimate: a measure of the error associated with predicting the value of x from the dependant observation y: sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi X 2ffi X 1 S¼ y n y2 nðn 2Þ 2 P P P n xy x y 2 P P n x2 x
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